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Biotechnology Advances 31 (2013) 11531171

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Biotechnology Advances
journal homepage: www.elsevier.com/locate/biotechadv

Research review paper

Phytohormones and microRNAs as sensors and regulators


of leaf senescence: Assigning macro roles to small molecules
Maryam Sarwat a,, Afsar Raza Naqvi b, Parvaiz Ahmad c,, Muhammad Ashraf d, Nudrat Aisha Akram e
a
Pharmaceutical Biotechnology, Amity Institute of Pharmacy, Amity University, Uttar Pradesh (AUUP), NOIDA, India
b
School of Dentistry, Department of Periodontics, University of North Carolina at Chapel, Hill, USA
c
Department of Botany, A. S. College, Srinagar, 190008, University of Kashmir, Srinagar, India
d
Department of Botany, University of Agriculture, Faisalabad, Pakistan
e
Department of Botany, GC University, Faisalabad, Pakistan

a r t i c l e i n f o a b s t r a c t

Article history: Ageing or senescence is an intricate and highly synchronized developmental phase in the life of plant parts includ-
Received 28 May 2012 ing leaf. Senescence not only means death of a plant part, but during this process, different macromolecules under-
Received in revised form 26 January 2013 go degradation and the resulting components are transported to other parts of the plant. During the period from
Accepted 2 February 2013 when a leaf is young and green to the stage when it senesces, a multitude of factors such as hormones, environ-
Available online 20 February 2013
mental factors and senescence associated genes (SAGs) are involved. Plant hormones including salicylic acid,
Keywords:
abscisic acid, jasmonic acid and ethylene advance leaf senescence, whereas others like cytokinins, gibberellins,
Leaf senescence and auxins delay this process. The environmental factors which generally affect plant development and growth,
Senescence associated genes (SAGs) can hasten senescence, the examples being nutrient dearth, water stress, pathogen attack, radiations, high temper-
Cytokinins ature and light intensity, waterlogging, and air, water or soil contamination. Other important inuences include
Ethylene carbohydrate accumulation and high carbon/nitrogen level. To date, although several genes involved in this com-
Auxins plex process have been identied, still not much information exists in the literature on the signalling mechanism of
PCD leaf senescence. Now, the Arabidopsis mutants have paved our way and opened new vistas to elucidate the signal-
MicroRNA
ling mechanism of leaf senescence for which various mutants are being utilized. Recent studies demonstrating the
Arabidopsis mutants
role of microRNAs in leaf senescence have reinforced our knowledge of this intricate process. This review provides
a comprehensive and critical analysis of the information gained particularly on the roles of several plant growth
regulators and microRNAs in regulation of leaf senescence.
2013 Elsevier Inc. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1154
1.1. Senescence, its roles and mechanism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1154
2. Regulation of leaf senescence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1155
2.1. Gene expression during senescence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1156
2.2. Perception and transduction of senescence signals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1156
2.3. Transcription regulation of gene expression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1157
3. Progression of senescence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1157
3.1. Chloroplast degradation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1157
3.2. Role of mitochondria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1158
3.3. Loss of membrane integrity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1158
4. Senescence and Programmed Cell Death (PCD) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1158
5. Involvement of phytohormones in leaf senescence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1159
5.1. Cytokinins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1159
5.2. Ethylene . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1159
5.3. ABA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1159
5.4. Jasmonic acid . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1163
5.5. Salicylic acid . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1163

Corresponding authors.
E-mail addresses: maryam21_7@yahoo.com (M. Sarwat), parvaizbot@yahoo.com (P. Ahmad).

0734-9750/$ see front matter 2013 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.biotechadv.2013.02.003
1154 M. Sarwat et al. / Biotechnology Advances 31 (2013) 11531171

5.6. Brassinosteroids (BRs) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1163


5.7. Auxins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1163
5.8. Gibberellins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1164
5.9. Polyamines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1164
6. Stress and senescence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1164
6.1. Role of transcription factors in regulation of leaf senescence under stress conditions . . . . . . . . . . . . . . . . . . . . . . . . 1165
6.2. Role of reactive oxygen species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1165
7. Micro RNA and senescence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1165
7.1. miR164 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1165
7.2. miR319 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1166
8. Conclusion and future prospects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1166
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1166

1. Introduction senescence, e.g., SEN1 gene observed in Arabidopsis, contribute signi-


cantly to leaf senescence during stresses (Schenk et al., 2005). Recently,
Normally, senescence is a synchronized series of events occurring in it has been shown that over-expression of the genes involved in cold ac-
plants during the course of development, but a stress of any type may climation like CBF2 and CBF3 delayed leaf senescence (Sharabi-Schwager
bring about senescence in plants much earlier than usual (Lim et al., et al., 2010).
2007; Lobell et al., 2012). The changes with time that fall under the gen- From all the above-mentioned reports it is amply clear that the se-
eral term ageing are not necessarily deteriorative, although in the long nescence phenomenon is very complex, which is regulated by a series
run errors will accumulate and living tissues will show signs of wear of metabolic events as well as genes. Thus, in the present review all
and tear. According to some proposed models, senescence is an acceler- factors responsible for causing or accelerating senescence have been
ated form of ageing. Ageing is a term, like senescence that has become comprehensively discussed. How far different phytohormones and
associated with deterioration referring to changes that occur with microRNAs participated signicantly to control senescence under
time (Thomas et al., 2003). Premature senescence can reduce the crop non-stress and stress conditions have also been explicitly described
productivity up to 50% and is one of the primary causes of crop losses in the review (Fig. 1).
worldwide (Navabpour et al., 2003).
In senescence, a series of metabolic events take place. For example, 1.1. Senescence, its roles and mechanism
leaf ageing is a synchronized and sequential process in which the chlo-
roplast rst undergoes degeneration, followed by hydrolysis and Senescence is an intricate but much regulated metabolic process. It
remobilization of macromolecules to other parts. Finally, disintegration goes on throughout the life of the plant. It involves synchronized mobi-
of nucleus as well as mitochondrion takes place (Buchanan-Wollaston lization of nutrients like nitrogen, carbon and minerals from senescing
et al., 2003, 2005; Wang, 2012). Furthermore, several genes have so tissues to other plant parts (Milla et al., 2007; Wang, 2012). Loss of chlo-
far been identied which are up- or down-regulated during senescence. rophyll and decrease in the total RNA and protein contents also take
For example, a study using ATH1 microarray taken from Arabidopsis ge- place during this deteriorative process (Diaz et al., 2005). Although
nome sequence has shown up-regulation of 303 and down-regulation the kinds of senescence reported are leaf, ower and fruit senescence,
of 81 transcription factors during dark-induced senescence (Lin and in this review we have emphasized mainly on leaf senescence.
Wu, 2004). Recently, a crucial role of some other genes such as NAC An interesting question arises here that how leaf senescence is initi-
family, WRKY53 TFs, WRKY6 and AtNAP, has been observed in leaf senes- ated and how the plant recognizes a particular developmental stage to
cence (Besseau et al., 2012; Sharabi-Schwager et al., 2010). initiate the senescence program. Some studies provide a clue that
Other factors inuencing leaf senescence include plant hormones. sugar concentration plays a considerable role in the coordination and
Hormones like, jasmonates (He et al., 2002), ethylene (Grbic and regulation of leaf senescence which specically depends on leaf photo-
Bleecker, 1995), salicylic acid (Morris et al., 2000) and ABA (Zeevaart synthetic capacity (Jang et al., 1997; Wingler et al., 2006). Others
and Creelman, 1988) promote leaf senescence, whereas others like cy- suggest reduced metabolic rate as a trigger during age-dependent se-
tokinins (Jung et al., 2006), gibberellins (Mutui et al., 2006) and auxins nescence, but not in dark- or hormone-induced senescence. For exam-
(Kim et al., 2011a) hinder senescence. Overall, all the environmental ple, in Arabidopsis mutants oresara 4-1 (ore4-1), a lesion in chloroplast
factors which cause deleterious effects on plant growth (Ahmad et al., functions resulted in reduced metabolic rate (Woo et al., 2002).
2008, 2010a, 2010b; Koyro et al., 2011) can speed up senescence The overall structure of the leaf cells changes as the senescence pro-
(Lers, 2007). Furthermore, carbohydrate accumulation and accessibility cess starts in them. However, the vascular system of the plant is
of high carbon to low nitrogen level represent other factors that can reg- maintained until the very late stages as it is required for the transporta-
ulate leaf ageing (Wingler et al., 2006). tion of nutrients from the senescing tissues into young tissues as well as
Studies on the elucidation of the mechanism of senescence in several reproductive organs like owers and seeds (Cholewa and Grifth, 2004;
aerobic organisms have led to an intriguing stress resistance theory of Fukuda, 1996; Wang, 2012).
ageing which indicated that improvement against stresses could delay Senescence effectively inuences the expression of certain genes
senescence thereby expanding the life span of plants (Pardon, 2007). involved in degradation of proteins into amino acids, RNA to low molec-
This is further supported by a study on Arabidopsis, where delayed- ular weight nitrogen compounds, and membrane lipids to fatty acids
leaf-senescence mutants including gigantea (gi-3), ore9, ore3 and ore1 and sugars (Buchanan-Wollaston, 1997; Zimmermann and Zentgraf,
have been found markedly tolerant to oxidative disorders (Cao et al., 2005). However, the DNA content remains unchanged till the very
2006; Woo et al., 2004). Furthermore, a possible coupling between leaf late stages of senescence and the DNA fragmentation is recorded at
senescence and stress responses has been described by Lim et al. the end phase (Campisi and Fagagna, 2007; Huna et al., 2011; Orzaez
(2007). Chen et al. (2002) showed an overlapping role of about 28 senes- and Granell, 1997). These are the inherent changes which take place
cence induced genes in tolerance to various stresses. This phenomenon during senescence. Furthermore, there are a number of factors which
has also been observed in the case of other genes have a key role in cause premature senescence, including environmental factors like
M. Sarwat et al. / Biotechnology Advances 31 (2013) 11531171 1155

Endogenous factors Environmental factors


Phytohormones Photoperiod
Reproduction Nutrient deficiencies
Plant age & size Salinity
Meristem indeterminacy Heat or cold
Light stress
Water stress
Ozone

Onset of Leaf Senescence


Initiation phase
[Shift in gene expression e.g. Senescence Associated Genes (SAGs); transduction of
senescence signals; over -accumulation of reactive oxygen species]

Re-organization phase
(Chlorophyll degradation; degradation of proteins, lipids and other macromolecules; nutrient
translocation by the phloem)

Terminal phase
(Cell deathdisruption of organelles)

Leaf abscision (Not always)


Fig. 1. Different factors involved in senescence (partially adopted from Munne-Bosch, 2008 with slight modication with permission).

abiotic e.g., nutrients deciency, drought, salinity, waterlogging, heat leaves (Izumi and Ishida, 2011). As the leaf grows, expands and pro-
stress and oxidative disorders caused by different stresses and biotic gresses towards senescence, the RCB production generally increases,
factors particularly pathogen attack to plants. whereas in the later stages of senescence, the RCB production drops
Worldwide, extensive research work on molecular biology of leaf and a large amount of carbohydrates accumulates, primarily glucose
senescence is being conducted on the model plant Arabidopsis and fructose.
thaliana because of its short life cycle, readily distinguishable devel- Chlorophyll degradation is a promising process during leaf senes-
opmental changes and reproducible senescence program, but such cence, which involves degradation of thylakoid membranes as well as
work in other plant species is not much yet. various chlorophyllprotein complexes. Plant mutants which retain
greenness by improving chlorophyll during leaf senescence are known
2. Regulation of leaf senescence as stay-green mutants. It has been reported that non-functional
stay-green mutants, defective in chlorophyll degradation, can effective-
Leaf senescence is a well-regulated phenomenon which takes place ly maintain greenness but not leaf functionality during senescence
through different genetically programmed events. It involves a myriad (Morita et al., 2009). A protein termed as STAYGREEN PROTEIN (SGR)
of physiological changes such as the increase in number of senescing is known to play a variety of physiological roles in plants particularly
leaves especially during owering and seed development. The aging during leaf senescence. For example, this protein can disassemble chlo-
leaves generally serve as a source of nutrients during reproduction, and rophyllprotein complexes in photosystem II and works together with
the nutrients which are stored in the seeds, serve as the reserve food photosystem II proteins (Aubry et al., 2008). In rice, the SGR has been
for the next generation. Furthermore, age of the leaf and subsequently reported to be absent from mature leaves (Zhou et al., 2011). Rice mu-
age of the plant is the most important endogenous factor which regulates tants lacking SGR have long-lived chloroplasts and SGR over-expressing
leaf senescence. As the plant gets older, its photosynthetic activity drops, lines show rapid degradation of chloroplasts in the developing leaves
and this can be contemplated as a senescence-inducing signal (Guo and (Park et al., 1998). The transcript level of SGR is specically induced
Gan, 2012; Mohapatra et al., 2010; Smart, 1994). In annual plants, photo- during leaf senescence (Park et al., 1998). SGR is a homolog of SGN1
synthetic rate of leaf shows a consistent decline after the full expansion in A. thaliana. Arabidopsis mutants acd2 (accelerated cell death 2) and
of the leaf (Hensel et al., 1993), however, it varies from species to species. acd1 (accelerated cell death 1) (Mach et al., 2001; Pruinsk et al.,
For example, in A. thaliana the leaves undergo fast-aging. A decline of al- 2003) lack SGN1 activity.
most 50% in its photosynthetic capacity has been observed within one The permeabilization of chloroplast membrane is a common event
week preceding full expansion of its leaves if kept under continuous that takes place during progression of senescence, but its mechanism is
light (Hensel et al., 1993). It is now evident that high amount of sugar still unknown. In animal system, arachidonic-type 15-lipoxygenases
down-regulates photosynthesis related genes (Bilgin et al., 2010; have been reported to be involved in the permeabilization of the outer
Chaves et al., 2009; Rolland et al., 2002). In fact, a close relationship has membranes of mitochondria, peroxisomes and ER particularly during
been reported between the autophagic degradation of chloroplasts differentiation of reticulocytes and keratinocytes (van Leyen et al.,
through rubisco-containing bodies (RCBs) and the carbon content of 1998). Similarly, we can assume the role of 13-LOX enzymes present in
1156 M. Sarwat et al. / Biotechnology Advances 31 (2013) 11531171

chloroplasts (Bell et al., 1995; Feussner et al., 1995; Nemchenko et al., as ARABIDOPSIS A-FIFTEEN (AAF) has been recently identied by
2006; Rangel et al., 2002; Seltmann et al., 2010) during plant senescence. Chen et al. (2012). The overexpression of AAF in Arabidopsis has
Furthermore, destruction of chloroplast may take place due to mem- been shown to promote leaf senescence. Products of these SAGs
brane fatty acid peroxidation (Blokhina et al., 2003; Kunz et al., 2009). cause degradation of a variety of macromolecules and remobilization
Senescence is naturally an irreversible process, which takes place of nutrients thereby speeding up the process of senescence. The com-
due to decrease in photosynthesis due to inactivation of rubisco, plex regulatory network of senescence involves an array of various
while activation of proteinase, lipid peroxidation and membrane metabolic pathways (Lim et al., 2007). One of those networks was
leakiness (Navabpour et al., 2003; Palma et al., 2002; Sato et al., recorded in Arabidopsis (He et al., 2001). A few years ago, while work-
2007). Generally, leaf protein and chlorophyll levels are considered ing with senescence leaves of Arabidopsis, Guo et al. (2004) have
as metabolic markers of leaf senescence. Expression of genes involved shown the involvement of 2500 genes as is evident from single pass
in protein synthesis and photosynthesis declines with an increase in sequencing of its cDNA library. Another study entailing the microar-
that of senescence-associated genes (SAGs) during senescence. More- ray analyses of Arabidopsis cDNAs has shown the change in the
over, Navabpour et al. (2003) reported that SAGs express in response expression of about 20% of the genes during leaf senescence
to enhanced production of ROS, because cellular oxidation is a key (Buchanan-Wollaston et al., 2003; Zentgraf et al., 2004). However, in-
phenomenon during leaf senescence (Chen and Dickman, 2004; formation on the regulation of these genes is not much in the litera-
Navabpour et al., 2003; Zentgraf and Hemleben, 2008). Generally, ture. Recently, TOR (target of rapamycin) is reported as a negative
the naturally rmly controlled balance between generation and regulator of leaf senescence (Dobrenel et al., 2011). It has been ob-
counteracting of ROS has been reported to be perturbed during the served that leaf and root biomass increases in plants overexpressing
progression of senescence in different cellular compartments either TOR. These plants produce more seeds and are more resistant to dif-
by reduction in antioxidants or excess generation of ROS (Dai et al., ferent stresses (Dobrenel et al., 2011). Targeted silencing of TOR by
2012; Zentgraf and Hemleben, 2008). RNAi (RNA interference) approach leads to a reduced organ growth
Recent genetic evidence suggests that ROS act as signals that acti- and early senescence accompanied by high accumulation of sugars
vate genetically programmed pathways of gene expression that regu- and amino acids (Dobrenel et al., 2011). Recently, Liu et al. (2011)
late cell suicide processes (Foyer and Noctor, 2005; Zentgraf and have generated a leaf senescence database (LSD, http://www.
Hemleben, 2008). Plants use ROS as second messengers in many signal eplantsenescence.org/) which comprises 1145 SAGs from 21 plant
transduction cascades from mitosis to PCD (Bhattacharjee, in press; species. They have categorized the SAGs based on their role in leaf se-
Foyer and Noctor, 2005; Vanacker et al., 2006), and thus ROS accumula- nescence. This site provides rich information to researchers working
tion is essential to plant development as well as defence. Similarly, the to elucidate the function and expression of different SAGs as well as
plant antioxidant defence network in the form of antioxidant com- explore the signalling network, and the origin and evolution of
pounds and antioxidant enzymes, is necessary in controlling the SAGs. It is expected that this database will expand considerably in
life-span of the ROS signals as well as in preventing uncontrolled cellu- the future as a number of groups are actively pursuing research on
lar oxidation. uncovering unidentied SAGs in different plant species.

2.1. Gene expression during senescence 2.2. Perception and transduction of senescence signals

As mentioned earlier, leaf senescence is under strict genetic control, Various factors including sugars, environmental stresses, and plant
and it requires several genes which express/repress in response to differ- growth regulators are involved in the perception and signalling of se-
ent metabolic processes, signalling pathways and transcription factor ac- nescence. The role of some of the phytohormones on signal transduc-
tivities (Gadjev et al., 2008; He et al., 2001; Lim et al., 2003; Tenea et al., tion in senescence are well studied, like ethylene (Klee, 2004), while
2011). All these trigger different biochemical/physiological processes. the research on other phytohormones is still in infancy.
Cell senescence is also associated with activation of the TOR (target of Various studies have revealed receptor kinases to serve as receivers
rapamycin) nutrient- and mitogen-sensing pathway, which promotes and/or transducers of intrinsic or extrinsic signals. For example, leaf se-
cell growth, even though cell cycle is blocked (Blagosklonny, 2011). Up nescence is reported to induce receptor like kinase (RLK) in tomato
till now, many senescence-associated genes (SAGs) have been identied (SARK) (Hajouj et al., 2000), lecRK a1 (Riou et al., 2002), SIRK
in different plant species. Gepstein et al. (2003) identied 70 genes stim- (Robatzek and Somssich, 2002), Paul27 in Populus tremula (Bhalerao et
ulating macromolecule degradation, detoxication of oxidative metabo- al., 2003) and At5g48380 in Arabidopsis (Gepstein et al., 2003). In
lites, induction of defense mechanisms, and signalling and other Arabidopsis alone, 610 RLK genes constitute a large gene family (Shiu
regulatory events during senescence. Li et al. (2012) developed a curated and Bleecker, 2003). Of them, 44 are found in senescing leaves (Guo et
database of genes potentially associated with leaf senescence, the Leaf al., 2004). To have a better detail of signal perception of leaf senescence
Senescence Database (LSD) and gene networks to identify common reg- functional study of these RLK genes is essential. Involvement of MAPK
ulators of leaf senescence in A. thaliana. They found that phytohormones signalling cascade in senescence was rst postulated by Guo et al.
play a critical role in regulating leaf senescence. Functional analysis of (2004) with the representation of 3 MAPKs, 3 MAPKKs, 9 MAPKKKs,
candidate SAGs in LSD revealed that a WRKY transcription factor and 1 MAPKKKK in one of the senescent leaf EST databases. MAPKs are
WRKY75 and a Cys2/His2-type transcription factor AZF2 are positive reg- also reported from other plant species, e.g., Paul31 from P. tremula
ulators of leaf senescence and loss-of-function of WRKY75 or AZF2 MAPK, EDR1 from Arabidopsis and zmMPK5 from maize. Paul31 is the
delays leaf senescence. During another study, Espinoza et al. (2007) most strongly expressed gene specic to autumn senescing in Populus
suggested that different virus-induced genes are also expressed at ele- leaves (Bhalerao et al., 2003). Li et al. (2006) cloned and characterized
vated levels during natural senescence in vigorous plants. They showed a receptor-like kinase (RLK) gene, GmSARK (Glycine max senescence-
the role of SAGs during compatible viral interactions in A. thaliana and associated receptor-like kinase) in soybean. This gene is reported to be
grapevine, and reported that SAGs encode proteins such as proteases, li- involved in regulating leaf senescence. ABA is considered as an
pases, and proteins involved in the mobilization of nutrients and min- up-regulator of leaf senescence. While elucidating the role of ABA in
erals, transporters, transcription factors, proteins related to translation, senescence signalling in Arabidopsis, Lee et al. (2011) have examined
and antioxidant enzymes. the role of an ABA-induced gene, RPK1, which induces leucine-rich
Recently, an SAG SPA15 has been identied in sweet potato repeat-containing receptor protein kinase 1. Furthermore, the authors
(Ipomoea batatas) but its function is still unknown. To elucidate the observed that rpk1 mutants showed decreased sensitivity to
role of SPA15 in leaf senescence, an orthologue of SPA15 referred to ABA-induced senescence, but they did not alter JA-or ethylene-induced
M. Sarwat et al. / Biotechnology Advances 31 (2013) 11531171 1157

senescence, conrming considerable responsiveness of RPK1 to ABA. The of WRKY53 can be stress related genes, defense-related genes, and
expression of RPK1 at different phases of growth was found to be some SAGs (Miao et al., 2004; Zhang et al., 2011; Zhou et al., 2011).
variable, being maximal at the adult stage, the stage at which senescence Arabidopsis WRKY transcription factors have been reported to partic-
process is generally accelerated. Tang and Innes (2002) reported ipate in the gene expression during trichome development, wounding
ethylene-induced senescence in Arabidopsis plants by over-expressing and pathogen defense along with senescence (Zhou et al., 2011). Tran-
kinase decient EDR1 gene. Some studies revealed involvement of calci- scription of WRKY22 was reported to be promoted by darkness and de-
um dependent protein kinases, calcium binding proteins, G proteins, creased by light. Over-expression of AtWRKY22 (dark-treated) and
protein phosphatases, and 14,3,3 proteins in leaf senescence (de Silva knockout lines indicated phenotypes with varying response to senes-
et al., 2011; Gepstein et al., 2003; Guo et al., 2004; Guterman et al., cence (Zhou et al., 2011). Furthermore, AtNAP is a NAC family transcrip-
2003). Thus, there is an indication of association of other signal transduc- tion factor gene that contributes signicantly in leaf senescence, but its
tion pathways such as calcium signalling, G protein mediated signalling, mechanism needs to be elucidated (Zhang et al., 2011).
phosphatases, and 14,3,3 proteins with leaf senescence. TCP is another transcription factor family involved in regulating leaf
Furthermore, nitric oxide (NO) and calcium (Ca 2+) also show their senescence (Guo et al., 2010; Pulido and Laufs, 2010). TCPs can be
vital role in plant senescence signalling cascade. Calcium (Ca 2+) can hin- grouped into class 1 and class 2 (Cubas et al., 1999; Kosugi and
der senescence, especially in detached leaves (Ma and Berkowitz, 2011; Ohashi, 2002). Interestingly, both differ in their effect on senescence
Poovaiah and Leopold, 1973). It has been observed that Ca2+ can defer regulation. Class 1 TCPs (e.g. TCP20) are positive regulators of growth,
methyl jasmonate (MeJA)-induced leaf senescence in rice (Ma and while in contrast, class 2 TCPs including TB1 and CYCDICH are negative
Berkowitz, 2011). During an investigation, overexpression of a bacterial regulators (Kosugi and Ohashi, 2002; Li et al., 2005; Uberti-Manassero
NO dioxygenase (NOD), which has a key role in detoxifying NO in trans- et al., 2012). Balance of these classes is necessary for proper growth of
genic Arabidopsis, resulted in premature leaf senescence. However, exog- organs. The class 2 TCP genes include CINCINNATA (CIN) and JAW-D
enous treatment of NO delayed early senescence occurring in transgenic (Palatnik et al., 2003). The gene CIN controls cell division arrest in
Arabidopsis NOD plants (Mishina et al., 2007). Recently, Ma and leaves. Thus, it is involved in senescence response. TCPs also exert
Berkowitz (2011) have shown that Arabidopsis cyclic nucleotide gated their effect by regulating WRKY53, and in turn onset of early senescence
channel 2 (CNGC2) has an important role in senescence signalling in- gene expression. ORE1 is another transcription factor which may bind
duced by calcium inux. The CNGC2 loss-of-function mutant dnd1 to the promoters of SAGs and cause their activation. ORE1 is regulated
resulted in decreased Ca 2+ uptake and early senescence have been ob- by ethylene-insensitive 2 (EIN2) and others in an age-dependent
served as compared to the wild type. In addition, endogenous NO con- manner.
tent in dnd1 leaves was less than that in the leaves of non-transgenic Another transcription factor RAV1 (RAV family) plays a key func-
lines. Thus, the present study suggests that NO is a negative regulator tion during initial events of leaf senescence (Woo et al., 2010; Zhao
and Ca2+ as a positive regulator in senescence signalling. et al., 2008). In a study, the role of RAV1 has been found to be closely
interlinked with leaf senescence. The RAV1 mRNA increased with age
2.3. Transcription regulation of gene expression and reached to a maximum level on the initiation of senescence, but
interestingly declined again at the nal stage of senescence which
Transcription is regulated by transcription factors, connected to def- suggested that RAV1 is a positive regulator of senescence and its ex-
inite cis-elements on the target gene promoters, which, in turn, cause pression is sufcient to cause leaf senescence (Woo et al., 2010).
differential gene expression by activation and/or suppression of their Similarly SAG113, a gene encoding a Golgi-localized PP2C family
respective genes. About 1500 transcription factor genes were reported protein phosphatase, regulates ABA-induced stomatal opening/closing
in the Arabidopsis genome, which altogether constitute more than 30 and dehydration, especially during leaf senescence (Zhang et al.,
gene families (Riechmann et al., 2000). Interestingly, more than 130 2011). Recently, Zhang et al. (2011) investigated that two genes namely
of them were reported from leaf senescence EST collection of SAG113 and AtNAP were over-expressed during ABA accumulation and
Arabidopsis (Guo et al., 2004). These senescence transcription factors leaf senescence. Overall, chemical induction of AtNAP also induces ex-
belong to the families of NAC, WRKY, AP2/EREBP, C2H2, C3H, C2C2, zinc pression of SAG113. However, when AtNAP was knocked out, the ABA-
nger proteins, MYB, HB, bZIP, and bHLH, etc. (Guo et al., 2004). Previ- and senescence-induced expression of SAG113 also decreased.
ously, Chen et al. (2002) also showed senescence induced expression of From all the above reports it is amply clear that a variety of tran-
43 genes out of 402 transcription factor genes on a microarray. scription factors exist in the leaves, which contributed signicantly
Among the best studied leaf senescence associated transcription fac- in the regulation of leaf senescence. However, different types of tran-
tors, WRKYs are the promising ones. The WRKY family is characterized of scription factors regulate the transcription phenomenon to a varying
possessing a 60 amino acid motif, the WRKY domain (Eulgem et al., extent thereby regulating leaf senescence variably. With further ad-
2000). Of these, two WRKY proteins including WRKY6 and WRKY53, vancement in knowledge on the interactive role of all such types of
have been found to be up-regulated during leaf senescence (Eulgem et transcription factors in regulating leaf senescence it would be possi-
al., 2000; Hinderhofer and Zentgraf, 2001). The AtWRKY6 exerts its effect ble to enhance crop yield by delaying stress-induced senescence.
by modulating calmodulin-response genes and other senescence-
induced kinases, known as SARK and SIRK (Robatzek and Somssich, 3. Progression of senescence
2002). SARK and SIRK show similarity in structure as they consist of a
SerThr kinase domain, a trans-membrane domain as well as an extra- 3.1. Chloroplast degradation
cellular leucine-rich domain (Yoshida, 2003). Further, Robatzek and
Somssich (2001, 2002) worked on Arabidopsis WRKY6 and SIRK expres- Senescence starts with the degradation of chloroplast (Hrtensteiner
sion during leaf senescence. It is well known that SIRK is a receptor and Krutler, 2011). It can be observed in the form of disorientation of
kinase, so WRKY6 binds to the promoter of SIRK and control its expres- granum stacks and swelling of the thylakoids resulting into plastoglobuli
sion. The WRKY6 positively regulates PR1 (a defense related gene that enlargement (Gan and Amasino, 1997; Smart, 1994; Thomas and
is also expressed during leaf senescence), possibly through its transcrip- Stoddart, 1980; Zentgraf and Hemleben, 2008; Zimmermann and
tion factor NPR1 (Zhou et al., 2000). Hinderhofer and Zentgraf (2001) Zentgraf, 2005). A variety of intrinsic as well as extrinsic factors like
have shown induction of WRKY53 at early stages of leaf senescence. Se- ageing and different types of stresses may trigger the senescence
nescence is reported to get speeded up if WRKY53 is over-expressed in program by causing loss in photosynthetic capacity or membrane
Arabidopsis plants and delayed when RNAi or insertional mutation integrity (Azad et al., 2008; Franklin et al., 2012; Quirino et al., 2000).
suppressed this gene (Miao et al., 2004). The downstream target genes The most important and widely occurring chloroplast protein,
1158 M. Sarwat et al. / Biotechnology Advances 31 (2013) 11531171

ribulose-1,5-bisphosphate carboxylase/oxygenase (rubisco) is rapidly deterioration caused by ROS-induced lipid peroxidation. Merzlyak and
and selectively degraded during senescence, however, the mechanism Hendry (1994) reported that membrane lipid peroxidation is one of
is still not fully known (Khanna-Chopra, 2011). During senescence, a the promising effects of senescence in plant leaves. While assessing
non-yellowing gene (NYE1) has been reported to be a key regulator of the inuence of salt stress on senescence-related attributes in rice seed-
leaf chlorosis (Ren et al., 2007; Wei et al., 2011). Similarly, in rice a lings Lutts et al. (1996) reported that increased membrane permeability
novel protein RLS1 was found to be up-regulated and caused chloroplast is one of the foremost symptoms of leaf senescence. The authors suc-
degradation during dark-induced leaf senescence (Wang, 2012). The cessfully discriminated different rice genotypes for their tolerance to
degrading chloroplast is termed as gerontoplast by some researchers salt stress using membrane permeability as a very efcient selection
(Matile et al., 1999; van Doorn and Yoshimoto, 2010). The chlorophyll criterion.
and degraded products are transferred to the cell vacuole (Borrmann et
al., 2009; Matile et al., 1999; Pruinsk et al., 2007), probably to detoxify 4. Senescence and Programmed Cell Death (PCD)
the cell from this potentially phototoxic pigment (Christ et al., 2012;
Hrtensteiner and Krutler, 2011). The mobilization of chloroplasts to First experimental study on programmed nature of PCD was
the vacuole is done by rubisco-containing bodies (RCBs), which are gen- carried-out in 1980s and 1990s (Bozhkov and Lam, 2011; Walbot et al.,
erally spherical in shape (Izumi and Ishida, 2011). 1983), although 20002010 is the most promising decade for the study
Despite the above changes taking place in the chloroplast during se- of PCD (Bozhkov and Lam, 2011). Many external and internal factors
nescence, the thylakoid membrane particularly its uidity and compo- are known to cause PCD in plants, which depend on the expression of
sition remains unaltered, but the membrane-bound electron transport various genes involved in this process. For example, two independent
system I and II stied greatly during senescence (Falqueto et al., 2009; stresses (heat treatment and by allowing the cultures to senesce)
Hutter et al., 2004). Thus, the measurement of loss of photochemical ca- have been reported to induce PCD in plants which occur due to
pacity (Fv/Fm; which reects the functionality of photosystem II) at a up-regulation of certain genes during both processes (Feliciano et al., in
particular growth stage is one of the most promising criteria to detect press; Guo and Gan, 2012). Such genes were considered to be involved
senescence at that particular stage of a plant (John et al., 1995; Lim et in all types of PCD and they may serve as markers for this process
al., 2007, 2010; Oh et al., 1996, 1997; Zimmermann and Zentgraf, 2005). (Elmore, 2007; Palavan-Unsal et al., 2005). Examples are oxidative
From all these reports it is amply clear that the degradation of stress-related genes (CSD1, CSD3, and GPX) cysteine proteinases, some
chloroplast is the rst promising intracellular symptom of senescence transcription factors, and hypersensitivity response (HR)-related genes
taking place in a leaf. Not only ultrastructure of a chloroplast is dam- (Al-Taweel et al., 2011; Gill and Tuteja, 2010; Swidzinski et al., 2004).
aged during senescence but several metabolites occurring in the chlo- In the case of leaf senescence, PCD is regulated by several active genetic
roplast are also affected. programs. Of the different types of cells in a leaf, the mesophyll cells are
the rst that are affected during leaf senescence which later proliferate to
3.2. Role of mitochondria other cell types and eventually to the whole leaf tissue (Desvoyes et al.,
2006). In this way, leaf senescence is different from other types of PCD
In animal systems, mitochondrion is the main organelle which plays (van Doorn and Woltering, 2004), as the former involves whole tissues
an important role in the regulation of programmed cell death (PCD), and the latter is limited to specic tissues and cells. Moreover, senes-
whereas in contrast, in plant cells, this commission is carried out by cence in the case of leaves occurs in patches and progresses slowly in
the chloroplast. In fact, the mitochondrial functions are maintained dur- comparison with other PCDs known.
ing the whole breakdown process of the cell so they provide metabolic This slow progression in senescence ensures effective transport of
energy until the late phase of senescence (Keech, 2011; Thomson and nutrients to other parts. Different studies have reported the typical
Plat-Aloia, 1987; Zapata et al., 2005; Zimmermann and Zentgraf, PCD like symptoms in the late phases of senescing leaves of Arabidopsis,
2005). From animal mitochondria, discharging of cytochrome c is a tobacco, etc. (Cao et al., 2003; Simeonova et al., 2000; Uzelac et al.,
key event during apoptosis (similar to PCD in plants) (Balk and 2008). Some of these effects are DNA laddering, chromatin condensa-
Leaver, 2001). This can be supported by a study in which it has been tion and vacuolar collapse. A study on barley has also revealed disinte-
shown that an impediment in the release of mitochondrial cytochrome gration of nuclear DNA (nDNA) and condensation of chromatin as parts
c caused inhibition in apoptosis in animal cells which is closely involved of PCD (Kolodziejek et al., 2007). A similar order of events, rst frag-
with the activity of mitochondrial hexokinase (Eckardt, 2006). Further- mentation and then chromatin condensation, has been reported during
more, Kim et al. (2006) found that mitochondrial hexokinase regulates senescence (Kolodziejek et al., 2007; Tripathi and Tuteja, 2007). Unlike
PCD in plants, e.g., in Nicotiana benthamiana, virus-induced gene silenc- senescence, PCD is not coordinated even in the neighbouring cells and
ing (VIGS) of Hxk1 induced PCD. Likewise, overexpression of mitochon- does not spread at the constant rate. It has been observed that in the ini-
drial hexokinases in Arabidopsis enhanced survival under PCD-inducing tial stage of senescence, the concentration of NO reaches to ceiling in the
conditions (Eckardt, 2006). However, in plants in addition to mitochon- cytoplasm of mesophyll cells and during later stages this concentration
dria, chloroplasts play a considerable role in controlling PCD due to declines, suggesting a vital role of NO signalling in induction of PCD (da
stress-induced over-production of ROS (Doyle et al., 2010). It is evident Silva et al., 2011; de Michele et al., 2009; Kolodziejek et al., 2007).
from a study with Arabidopsis that antioxidant treatment enhanced PCD Although senescence is a type of PCD (van Doorn and Woltering,
induction, revealing that there is a composite interaction among chloro- 2004), its properties differ from those of PCD (Thomas et al., 2003). As
plasts, nuclear protein synthesis, light and ROS during plant PCD (Doyle stated earlier, senescence involves degradation of macromolecules like
et al., 2010). DNA, RNA and proteins and mobilization of carbon, nitrogen, phospho-
rus and other minerals within the plant body (Fischer, 2007). Senes-
3.3. Loss of membrane integrity cence has been reported to have a close link with PCD because of the
reason that the key hydrolytic enzymes (proteases and nucleases) in-
The loss of membrane integrity is an important aspect of the senes- volved in the breakdown of macromolecules are encoded by different
cence program. Due to this phenomenon mobilization of membrane senescence associated genes (SAGs) (Farage-Barhom et al., 2011). Var-
lipids takes place which is contemplated as crucial for providing energy ious studies conrm the up-regulation of these endonucleases during
for senescence to take place (Lim et al., 2007; Thompson et al., 1998). the course of senescence (like BFN1) (Farage-Barhom et al., 2008,
The release of lipids in this way results in increased membrane perme- 2011) and PCD (like ZEN1) (Ito and Fukuda, 2002). Moreover, the pro-
ability. Long ago, Dhindsa et al. (1981) reported that leaf senescence in tein sequences of senescence associated nuclease BFN1 are highly sim-
Nicotiana tabacum could be due to the effect of cumulative membrane ilar to ZEN1, a PCD-related nuclease (Ito and Fukuda, 2002). Both can be
M. Sarwat et al. / Biotechnology Advances 31 (2013) 11531171 1159

grouped into type I nuclease family. These are single-strand-specic accelerates leaf senescence. Isopentenyl transferase (IPT) is a key en-
endonucleases, like S1 nuclease which can degrade both RNA zyme in the biosynthesis of cytokinins, which also plays a signicant
and single-stranded DNA (Desai and Shankar, 2003). Different environ- role in delaying leaf senescence. But, the double transgenic tomato
mental factors can induce endonucleases (Muramoto et al., 1999; plants overexpressing both AtHXK1 and IPT show early senescence
Saumonneau et al., 2012; Yupsanis et al., 2001). Enhanced nuclease ac- phenotype (Swartzberg et al., 2011). This indicates the dominant nature
tivity has been reported during different phases of leaf senescence of AtHXK1 gene and so dominance of intracellular sugar sensing via
(Aleksandrushkina et al., 2008; Farage-Barhom et al., 2011). A variety AtHXK1 over extracellular sugar sensing mediated by IPT (Swartzberg
of other PCD processes like hypersensitive response (HR), aleurone et al., 2011). This indicates the complexities of hormonal signalling dur-
cell death, endosperm development, and tracheary element (TE) differ- ing senescence.
entiation have also been reported to be controlled due to up-regulation Cytokinins also mediate their action by modulating a number of
of nucleases (Dominguez et al., 2004; Farage-Barhom et al., 2008, 2011). transcription factor genes like GATA22, HAT4, HAT22 and bHLH64
Although involvement of mitochondria has not been conrmed in (Kllmer et al., 2011; Wang, 2012). For example, overexpression of
the programmed cell death (PCD) of leaf senescence, Swidzinski et al. HAT22 has been shown to cause reduction in chlorophyll content of
(2004) have reported down-regulation of the mitochondrial adenine seedlings and an early onset of leaf senescence in these plants
nucleotide transporter, suggesting an early event in the occurrence of (Kllmer et al., 2011). Further studies on the various transcription
plant PCD. Recently, in a comprehensive review, Bozhkov and Lam factor genes listed here or discovered in future may elucidate the
(2011) stated comparative analyses of cell death mechanisms in mechanism of leaf senescence.
plants, animals and fungi will provide an evolutionary framework
for understanding PCD function and control in various biological 5.2. Ethylene
systems as well as improvement in biomass and wood production,
disease and stress resistance. Signicant results in this eld will pro- While cytokinins suppress senescence, ethylene is known since
vide great impact on agriculture and forestry to cope with the long for hastening leaf senescence (Abeles et al., 1988). The underly-
ever-increasing demand for food production. ing genetic mechanism is beginning to be unravelled with studies fo-
cusing on genes of the ethylene biosynthetic pathway. The three
5. Involvement of phytohormones in leaf senescence major genes encoding ACC synthase, ACC oxidase and nitrilase are
reported to be up-regulated in many plant species during leaf senes-
Hormonal regulation of senescence is an interesting topic in its cence (Hirose et al., 2008; Van der Graaff et al., 2006). Further conr-
own right as it involves a complex interplay of signalling molecules mation came from some Arabidopsis mutant studies. For example,
at various stages of leaf senescence. Global expression proling and two mutants, ethylene-insensitive 2 (ein2) and ethylene-resistant 1
availability of genetic mutants have paved the way to unravel the (etr1), being decient in ethylene signal transduction, delayed leaf se-
mystery of these remarkable biomolecules and their role in senes- nescence (Lim et al., 2007). It was observed that leaf senescence did
cence (Table 1). not appear earlier in transgenic plants constitutively overproducing
ethylene (Lim et al., 2007; Yang et al., 2008). This suggests that ethyl-
5.1. Cytokinins ene alone cannot drive leaf aging.
Certain age-dependent factors are found to be a part of ethylene-
Of the various plant hormones studied for their role in senescence, regulated leaf senescence. In Arabidopsis the old1 (onset of leaf death
cytokinins receive the maximum attention, because of their consider- 1) mutant shows an earlier-onset of senescence (Jing et al., 2002). In
able role in delaying leaf-senescence (Kim et al., 2006; Lara et al., combination with ethylene, these mutants exhibit further accelera-
2004; Richmond and Lang, 1957; Xu and Huang, 2009). Thus, they tion of senescence. In the old1etr1 double mutant where ETR1 gene
are of great benet for the economically important plants. The levels is also mutated, ethylene perception was impaired (Gan, 2003;
of cytokinins within a cell gradually decline as leaf senescence pro- Lim et al., 2007). Thus, despite showing age-dependent early onset
gresses, and there is a general consensus that high levels of cellular of leaf senescence, there is no acceleration when treated with
cytokinins delay leaf senescence (Kim et al., 2006; Lara et al., 2004; ethylene.
McCabe et al., 2001). To further reinforce this observation, certain
studies (Frebort et al., 2011; Hirose et al., 2008; Xu et al., 2010) 5.3. ABA
have demonstrated the down-regulation of cytokinin biosynthesis
genes such as adenosine phosphate isopentenyl-transferase (IPT) The role of ABA in plant development as well as leaf senescence
and cytokinin synthase as well as up-regulation of cytokinin oxida- is well known (Table 1). Exogenous application of ABA has long
tion genes (cytokinin oxidase) during leaf senescence (Table 1). been known to promote leaf abscission and senescence (Zeevaart
The gain-of-function analysis of Arabidopsis ore12-1 mutant shows and Creelman, 1988). The level of ABA certainly increases in
insight into the molecular mechanism of cytokinin-mediated delayed senescing leaves and the exogenous application of ABA induces ex-
senescence response (Kim et al., 2006; Lim et al., 2007, 2010). Its pression of several SAGs (Choi and Hwang, 2011; Lim et al., 2007;
loss-of-function mutant AHK3 (Arabidopsis Histidine Kinase 3) causes Weaver et al., 1998). The correlation between ABA and senescence
reduced sensitivity to cytokinins thereby prompting senescence even is further conrmed by the up-regulation of both ABA and leaf se-
in the presence of cytokinins. The gene AHK3 possibly exerts its effect nescence during environmental stresses (drought, high salinity
by phosphorylating the Arabidopsis response regulator 2 (ARR2) and low temperature) (Tuteja, 2007). For gaining insight into the
(Horak et al., 2008; Kudryakova et al., 2008). cellular mediators of ABA-induced senescence, ABA inducible
The exact mechanism how cytokinins prevent senescence in receptor-like kinase gene of Arabidopsis, RPK1 has been comprehen-
the plant is not known. However, a correlation between cytokinins sively studied (Lee et al., 2011). Its expression increases during the
and the enzyme extracellular invertase has been reported (Lara et progression of leaf senescence. Loss-of-function mutants in RPK1
al., 2004). With the inhibition of extracellular invertase activity, showed delayed natural senescence. Interestingly, these mutants
cytokinin-regulated postponement in leaf senescence is also repressed, show reduced sensitivity to ABA-induced senescence, but little
which suggests the vital role of this enzyme in cytokinin-induced delay change to JA- or ethylene-induced senescence (Lee et al., 2011).
in leaf senescence. Furthermore, invertase activity enhances during The role of RPK1 in leaf senescence depends upon developmental
carbohydrate partitioning, which acts as a trigger for leaf senescence. stage of a leaf. Over-expression of RPK1 at an early stage causes
In contrast, another hexokinase AtHXK1, an intracellular enzyme, growth retardation but not senescence, while during adult stages
1160 M. Sarwat et al. / Biotechnology Advances 31 (2013) 11531171

Table 1
Role of different phytohormones in regulation of plant senescence.

Phytohormones Plant species Effect Reference

Cytokinins Rose (Rosa spp.) Application of the cytokinin (N6-henzyladenine) prolonged existence of fresh or aged Mayak and Halevy, 1970
owers of a short-lived rose variety, which shows that cytokinins take part in the
endogenous regulation of senescence in rose petals
Tobbaco (Nicotiana tabacum) In cytokinin-induced transgenic tobacco plants the production of cytokinins in Wingler et al., 1998
senescing tissue suppressed the rubisco, hydroxypyruvate reductase (HPR), and
some other enzymes participated in photosynthetic processes, which caused
delay in senescence, which might be due to reduction in photosynthesis-involved
proteins
Tobbaco (Nicotiana tabacum) Exogenous application of cytokinins increased its endogenous concentration which delayed Lara et al., 2004
senescence and caused nutrient mobilization
Petunia (Petunia hybrida Overproduction of cytokinins in petunia owers transformed with PSAG12-IPT delayed Chang et al., 2003
corolla senescence and reduced sensitivity to ethylene
Carnation (Dianthus Stem and leaf tissues of carnation (Dianthus caryophyllus) plants appeared to contain a Eisinger, 1977
caryophyllus) natural antisenescence factor (kinetin), and removal of these tissues from carnation
owers promoted senescence. However, exogenous application of kinetin (510 g/ml)
considerably delayed senescence of owers on removal of stem and leaf tissues. In
addition, the life span of cut-owers was increased with kinetin treatment
Tomato (Lycopersicon Over-expression of two (SAG12 and SAG13) senescence-associated Arabidopsis genes in Swartzberg et al., 2011
esculentum) tomato plants expressing isopentenyl transferase (IPT) causes delay in leaf senescence
and promotes owering
Creeping bentgrass Creeping bentgrass transformed with SAG12-ipt showed greater tiller as well as root Xu and Huang, 2009
(Agrostis stolonifera) formation and restricted leaf senescence under high temperature stress
Agrostis stolonifera The transformation of ipt (adenine isopentenyl transferase gene) regulating CK synthesis in Xu et al., 2010
a C3 perennial grass species, Agrostis stolonifera resulted in delayed senescence due to
change in protein contents and energy metabolism
Arabidopsis thaliana Loss-of-function mutant AHK3 (Arabidopsis Histidine Kinase 3) caused reduced Horak et al., 2008
sensitivity to cytokinins thereby prompting senescence even in the presence of
cytokinins. The gene AHK3 possibly exerted its effect by phosphorylating the
Arabidopsis response regulator 2 (ARR2)
Arabidopsis thaliana Expression of four different cytokinin-regulated transcription factor genes, GATA22, Kllmer et al., 2011
HAT4, HAT22 and bHLH64 has shown that of all the genes, overexpression of HAT22
lowered the seedling chlorophyll content and induced premature leaf senescence
Tomato The double transgenic tomato plants over-expressing both AtHXK1 and IPT appeared as Swartzberg et al., 2011
(Lycopersicon esculentum) an early senescence phenotype
Arabidopsis thaliana ARR5-gene expression in natural leaf senescence and detached leaf senescence in the Kudryakova et al., 2008
dark using Arabidopsis thaliana plants overexpressing PARR5-GUS gene showed that
natural leaf senescence was dependent on decreased GUS-activity
Auxins Arabidopsis thaliana Auxin response factors (ARFs) known as transcription factors regulate plant responses Ellis et al., 2005
to auxins. It has been found that arf2 mutant plants delayed rosette plant aging,
senescence and owering
Tobacco (Nicotiana tabacum) Transgenic lines showed greater lateral branches as well as prolonged preservation of Khodakovskaya et al., 2006
chlorophyll under dark incubation
Tropaeolum majus Roles of naphthalene acetic acid (NAA), indole butyric acid (IBA) and indole acetic acid Karatas et al., 2010
(IAA) were investigated on some physiological processes under dark-induced
senescence in Tropaeolum majus. IAA accelerated chlorophyll and carotenoid loss, while
improved protein contents
Arabidopsis thaliana Two allelic mutations, ore14-1 and ore14-2 induced a signicant delay in different Lim et al., 2010
senescence related attributes. Overexpression of ORE14 showed that it encodes ARF2, a
member of the auxin response factor (ARF), which mediated early auxin-induced gene
expression thereby positively regulating the leaf senescence in Arabidopsis
Arabidopsis thaliana Auxins cause down-regulation of over a half of the genes (IAA-TPs and AUX/IAA) of Van der Graaff et al., 2006
auxin transport which may result in uneven distribution of auxins
Arabidopsis thaliana Characterization of three arf2 mutants such as arf2-7, arf2-6 and arf2-8 causes delayed Okushima et al., 2005
owering, dark green rosette leaves, long and thick inorescence and sterility in early
appeared owers as well as delayed senescence and abscission, as compared to
wild-type plants
Arabidopsis thaliana Arabidopsis plants over-expressing YUCCA6 (a family of avin monooxygenase proteins) Kim et al., 2011a
displayed dramatic longevity, exhibited delayed dark-and hormone-induced senescence
Arabidopsis thaliana Transgenic plants overexpressing GmSARK, led to early leaf senescence, chloroplast Xu et al., 2011
degradation and alteration in ower morphology
Ethylene Watercress (Nasturtium spp.) While observing the efcacy of various inhibitors of ethylene synthesis such as Philosoph-Hadas et al., 1994
aminoethoxyvinylglycine (AVG), CO2 and Ag+ in retarding senescence processes it was
observed that application of CO2 (11%) to watercress bunches signicantly retarded the
senescence process. In addition, exogenous treatment of AVG (0.1 mM) or Ag+ (30 M)
to detached leaves signicantly reduced chlorophyll contents as compared to that of
proteolysis which showed that the delayed senescence cannot be associated only to its
action as an anti-ethylene agent. Therefore, it can be suggested that all
senescence-associated processes are not regulated by ethylene
Nicotiana sylvestris Transgenic N. sylvestris plants expressing Arabidopsis mutant ethylene receptor ETR1-1 Yang et al., 2008
or the tomato EIN3-like (LeEIL1) gene show time-course leaf senescence in transgenic
lines as compared to wild type plants. However, petal necrosis was delayed, These
observations support a role for ethylene in regulating a spectrum of developmental
events associated with organ senescence and tissue necrosis
Arabidopsis thaliana The association between age and ethylene to induce leaf senescence was observed in Jing et al., 2005
different accessions and mutants of Arabidopsis. Prolonged exposure of ethylene
M. Sarwat et al. / Biotechnology Advances 31 (2013) 11531171 1161

Table 1 (continued)
Phytohormones Plant species Effect Reference

enhanced the yellowing of leaves suggesting that leaf senescence also depends on the
duration of ethylene application
Petunia (Petunia spp.) Ethylene caused premature senescence of leaves and owers Jones and Pasian, 2011
Arabidopsis thaliana Senescence-associated receptor-like kinase (SARK), a leucine-rich repeat-receptor-like Xu et al., 2011
protein kinase, obtained from Glycine max acts as a positive regulator of leaf senescence.
Transgenic A. thaliana plants for inducible overexpression of GmSARK, led to early leaf
senescence, chloroplast destruction, and abnormal ower morphology. Inhibition of
ethylene biosynthesis alleviated the senescence-induced by GmSARK
Nicotiana mutabilis Up-regulation of 1-aminocyclopropane-1-carboxylic acid oxidase (ACO) transcripts Macnisha et al., 2010
elevated the rates of ethylene production at the onset of petal wilting
Hibiscus rosa-sinensis Flowers treated with 1-aminocyclopropane-1-carboxylic acid (ACC), a precursor of Trivellini et al., 2011
ethylene biosynthesis, enhanced ower senescence
Arabidopsis thaliana Interaction between leaf age and ethylene was assessed in isolated mutants with altered Jing et al., 2002
leaf senescence referred to as onset oeafdeath (old) mutants. The old1 is represented by
three recessive alleles and displayed earlier senescence both in air and upon ethylene
exposure. Analyses of the chlorophyll degradation, ion leakage and SAG expression showed
that leaf senescence was enhanced in ethylene-treated plants
Arabidopsis thaliana Ethylene-insensitive mutant etr2-1 shows leaf expansion, etiolated seedlings and leaf Sakai et al., 1998
senescence
Arabidopsis thaliana Ethylene insensitivity was conferred by ETR1 gene which promoted ethylene signal Chang et al., 1993
transduction pathway of Arabidopsis thaliana
Tomato (Lycopersicon Ethylene-induced the triple response in etiolated hypocotyls of various tomato Lanahan et al., 1994
esculentum) mutants except for Never ripe (Nr). Lack of ripening in this mutant was found to be
caused by ethylene insensitivity. In addition, overexpression of
1-aminocyclopropane-1-carboxylate (ACC) synthase in plants indicated that
they are phenotypically opposites of Nr plants
Nemesia strumosa Over-expression of ethylene receptor gene Cm-ETR1/H69A declined ethylene sensitivity Cui et al., 2004
in Nemesia strumosa. All the transgenic plants showed enhanced ower longevity as
compared to that of the wild types
Salicylic acid Arabidopsis thaliana The atg mutant phenotypes promote PCD. It was found that the cell death in the atg Yoshimoto et al., 2009
(SA) mutants is associated with SA signal
Arabidopsis thaliana Senescence-induced expression of the cysteine protease gene SAG12 was dependent on Morris et al., 2000
the presence of SA. In addition, delayed yellowing and declined necrosis in the mutant
plants defective in SA suggest a key role of SA in plant cell death
Arabidopsis thaliana Transgenic Arabidopsis overexpressing ACBP3 (ACBP3-OEs) displayed accelerated leaf Xiao et al., 2010
senescence. Furthermore, enhanced senescence in ACBP3-OEs transgenic plants depends
on SA, but not on jasmonates
Arabidopsis thaliana WRKY53 and WRKY70 were previously implicated as positive and negative regulators of Besseau et al., 2012
senescence, respectively. Involvement of two additional WRKY TFs, WRKY 54 and
WRKY30, has also been suggested in this process. Expression in wild-type and salicylic
acid-decient mutants suggests a common but not exclusive role for SA in induction of
WRKY30, 53, 54, and 70 during senescence which showed that WRKY53, WRKY54, and
WRKY70 may participate in a regulatory network that integrates internal and
environmental factors to modulate the onset and the progression of leaf senescence,
possibly through an interaction with WRKY30
ABA Arabidopsis thaliana Arabidopsis mutant oresara9 (ore9) leaf showed prolonged longevity during natural Woo et al., 2001
senescence by delaying the commencement of different senescence symptoms
Arabidopsis thaliana It has been believed that a senescing leaf loses water greater as compared to a Zhang et al., 2011
non-senescing leaf, and ABA has a prominent role in enhancing leaf senescence. They
identied a leaf senescence associated gene, SAG113, which is usually expressed in
senescing leaves and is induced by ABA. However, over-expression of SAG113 was
declined in aba2 and abi4 mutants
Arabidopsis thaliana Leaf senescence mutants [ore1 (oresara1), ore3 and ore9] show delayed senescence Kim et al., 2011b
phenotypes in dark-induced and age-dependent senescence. So, it is suggested that
ORE1, ORE3 and ORE9 can be used for the appropriate progression of leaf senescence
mediated by ABA as well as MeJA and ethylene
Cotton (Gossypium spp.) Leaf senescence is closely associated with reduced accumulation of zeatin and its Dong et al., 2008
riboside (Z + ZR) and isopentenyl and its adenine (iP + iPA) rather than enhanced ABA
or dihydrozeatin and its riboside (DHZ + DHZR) in cotton leaves
Arabidopsis thaliana Abscisic acid (ABA)-responsive NAC transcription factor VND-INTERACTING2 (VNI2) Yang et al., 2011
integrates ABA-induced stress signals into leaf aging by regulating RESPONSIVE TO
DEHYDRATION (RD) and COLD-REGULATED (COR) genes
Arabidopsis thaliana Age-dependent senescence was signicantly delayed in RPK1 decient mutants. Lee et al., 2011
However, overexpression of RPK1 at the reproductive stage signicantly enhanced the
senescence as well as cell death. Furthermore, induction of RPK1 at an early growth
stage reduced growth without generating senescence symptoms, which indicates that
the role of RPK1 in senescence is age dependent
Jasmonic acid Rice (Oryza sativa) A new zinc nger protein, OsDOS delays leaf senescence in rice. It is observed that Kong et al., 2006
(JA) expression of OsDOS was down-regulated during leaf senescence, pollination as well as
panicle development. RNAi knockdown of OsDOS increased age-dependent leaf
senescence, while its over-expression caused a considerable delay in leaf senescence,
which indicates that it acts as a negative regulator of leaf senescence
Cucurbita pepo Foliar-applied 100 M methyl jasmonate (MeJA) reduced chlorophyll content, Ananieva et al., 2007
chloroplast transcriptional activity and photosynthetic rate more than did by
darkness. This indicates that MeJA is a more potent inducer of senescence in
C. pepo seedlings

(continued on next page)


1162 M. Sarwat et al. / Biotechnology Advances 31 (2013) 11531171

Table 1 (continued)
Phytohormones Plant species Effect Reference

Jasmonic acid Arabidopsis thaliana JA induced premature senescence in detached as well as attached leaves in wild-type He et al., 2002
(JA) Arabidopsis indicating that JA-signalling is essential for JA to induce leaf senescence
Arabidopsis thaliana Exogenous application of JA enhanced leaf senescence in both drought sensitive and Yun-xia et al., 2010
drought tolerant genotypes and it was signicantly attributed to chlorophyll reduction
as well as increased malondialdehyde (MDA) contents
Arabidopsis thaliana TCP (TEOSINTE BRANCHED/CYCLOIDEA/PCF) transcription factor genes modulate Schommer et al., 2008
hormone responses including biosynthesis of JA. It was shown that miR319-controlled
TCP transcription factors coordinated two sequential processes in leaf development as
well as leaf growth, which was in fact down-regulated, while, in contrast, leaf
senescence was positively regulated
Arabidopsis thaliana Senescence-associated genes were identied in which the reporter gene GUS is He and Gan, 2003
up-regulated by both senescence and JA. Consistent with the GUS expression data,
another gene OPR1 was indeed up-regulated by both senescence and JA, which
suggests that leaf senescence and JA may share a common molecular mechanism
for modulating OPR1
Arabidopsis thaliana Exogenous application of MeJA caused increased expression of SAGs such as SEN4, SEN5, Xiao et al., 2004
and VPE and loss of chlorophyll content and photochemical efciency in Arabidopsis.
Mutant studies have further conrmed the role of JA in leaf senescence as JA-induced
senescence is absent in JA-insensitive mutant
Arabidopsis thaliana The 35 coronatine insensitive 1 (COI1)-dependent JA-regulated proteins were identied Shan et al., 2011
in Arabidopsis. Of them, Rubisco activase (RCA) was a COI1-dependent JA-repressed
protein. Furthermore, loss of RCA caused premature senescence
Brassinosteroids Arabidopsis thaliana Mutants decient in BR biosynthesis (det2) or the BR receptor BRI1 exhibited delayed Yang et al., 2011
(BRs) senescence, indicating that BRs are positive regulator of senescence
Arabidopsis thaliana BRI1-associated kinase 1 (BAK1) has a key role in BR signalling as well as Jeong et al., 2010
BR-independent plant defense response. Transgenic Arabidopsis plants expressing
BAK7 showed growth reduction and early senescence
Jujube (Ziziphus jujuba) Exogenous application of BRs (5 M) effectively enhanced the activities of superoxide Zhu et al., 2010
dismutase (SOD), phenylalanine ammonia-lyase, polyphenoloxidase as well as catalase
and delayed fruit senescence and maintained fruit quality by reducing ethylene
production
Wheat (Triticum aestivum) Exogenously-applied epibrassinolide (eBL) at the rate of 10 and 0.1 M accelerated leaf Salam-a, 2007
senescence in wheat plants due to increased peroxidase activity and decreased protease
activity and chlorophyll contents
Tomato (Lycopersicon Exogenous application of BRs to pericarp discs resulted in enhanced lycopene contents Vardhini and Rao, 2002
esculentum) and decreased chlorophyll pigments. In addition, it decreased ascorbic acid, while
increased carbohydrate contents. BR-induced fruit ripening was associated with
increased ethylene production, resulting in acceleration of fruit-senescence
Gibberellins Paris polyphylla Application of gibberellic acid (GA3) considerably enhanced the endogenous GAs Li et al., 2010
(GA4 + GA7) level and slowed down the senescence of shoots, and the degradation of
proteins and chlorophyll. While activities of chlorophyllase, Mg-dechelation and
peroxidase increased more in control plants than in those treated with GA3
Paris polyphylla Foliar-applied gibberellin A3 (GA3) showed antagonistic effects of GA and ABA on Yu et al., 2009
senescence
Zoysiagrass (Zoysia japonica) The seedlings treated with GA3 delayed leaf senescence induced by darkness Cheng et al., 2009
Tomato (Lycopersicon When leaf discs of tomato were treated with solutions containing GA3 (4.33 106 M), Parmar and Hammond, 1971
esculentum) senescence was retarded as compared to that in non-treated plants due to delay in
degradation of chlorophyll, and improved levels of total protein, RNA, and DNA
Taraxacum megallorrhizon, ABA reduced the senescence retarding effect of GA on excised leaf discs of the three plant Back and Richmond, 1971
Rumex pulcber species more than that of cytokinins. In addition, GA did not reverse the effects of ABA
and Tropaeolum majus
Pea (Pisum sativum) GA3 application in vitro resulted in rapid accumulation of GDA-1 mRNA in LD-grown G2 Li et al., 1998
pea apical buds, which is compatible with its delaying effect on apical senescence
Pea (Pisum sativum) The G2 line of pea exhibited apical senescence-delaying phenotype under short-day
(SD) conditions. The initiation of cell death signals in the terminal oral meristem was
involved in the regulation of apical senescence in pea plants
Polyamines Oat (Avena sativa) Foliar-applied diaminopropane, spermidine and spermine enhanced the chlorophyll Borrell et al., 1997
contents, while decreased malondialdehyde (MDA) levels, lipoxygenase activity as
well as enzyme-protein levels, which induced anti-senescence effects
Rosa bourboniana and Polyamine biosynthetic inhibitors diuoromethylornithine (DFMO), Sood and Nagar, 2008
Rosa damascena diuoromethylarginine (DFMA) and methylglyoxal-bis(guanylhydrazone) (MGBG)
enhanced senescence, however, exogenously-applied spermine considerably delayed
this phenomenon
Tobacco (Nicotiana tabacum) In excised owers, foliar-applied spermine caused an increase in free and acid-soluble Serani-Fracassini et al., 2002
conjugated PAs levels, resulting in delayed programmed cell death as well as senescence
Barley (Hordeum vulgare) The kinetin conserved low TGase levels/activity during leaf senescence which showed a Sobieszczuk-Nowicka et al.,
key component of the kinetin action in retarding leaf senescence 2009
Lactuca sativa Spermidine declined chlorophyll degradation and promoted endogenous TGase activity. Serani-Fracassini et al., 2010
However, exogenously applied TGase enhanced chlorophyll synthesis three-fold. The
senescence-delaying effects of spermidine were found to be regulated by TGase
Peach (Prunus persica) Field applications of spermidine (1 mM) on peach fruit showed reduced ethylene level Torrigiani et al., 2012
and esh softening. The endogenous concentration of free as well as insoluble
conjugated PAs increased 0.32.6-fold, while it caused reduction in non-treated plants
which showed that spermidine impedes fruit development as well as fruit ripening by
interacting with multiple hormonal pathways
Apple (Malus domestica) Methylglyoxal bis-(guanylhydrazone) (MGBG)-treated fruit had higher ethylene Pang et al., 2010
production as compared to that by non-treated fruits. The expression of apple
M. Sarwat et al. / Biotechnology Advances 31 (2013) 11531171 1163

Table 1 (continued)
Phytohormones Plant species Effect Reference

SAM synthase (MdSAMS) in MGBG-treated fruit was slightly higher than that in control.
In addition, considerable changes in free polyamine contents indicated a relationship
between polyamine and ethylene pathways
Tomato (Lycopersicon Over-expression of ySpdSyn (yeast spermidine synthase) in tomato enhanced Nambeesan et al., 2010
esculentum) intracellular
level of spermidine in the leaf as well as in the fruits. Furthermore, ySpdSyn transgenic
fruits had a longer shelf life, reduced shriveling and delayed senescence as compared to
non-transgenic plant fruits

senescence is accelerated thereby leading to cell death (Lee et al., 5.6. Brassinosteroids (BRs)
2011; Osakabe et al., 2010). Similar response is noticed for exoge-
nous application of ABA, which does not have an effect on young BRs are generally known as positive regulators of senescence. For
leaves but causes senescence in older leaves (Lee et al., 2011; Park example, mutants decient in BR biosynthesis (det2) or the BR receptor
et al., 1998). This indicates that ABA function in senescence is medi- BRI1 exhibit delayed senescence (Yang et al., 2011). However, contrari-
ated by RPK1. ly, the microarray expression proling has shown no effect on the ex-
pression of BR biosynthesis genes during senescence (Van der Graaff
5.4. Jasmonic acid et al., 2006). AtBRL3 is a BR receptor that functions in vascular differen-
tiation (Cano-Delgado et al., 2004). The signicant up-regulation of the
The positive role of methyl jasmonate (MeJA) and its precursor gene of this receptor during senescence supports the notion that BRs
jasmonic acid (JA) in leaf senescence has been well documented in a might function in controlling the vascular system for efcient transport
number of plants like Arabidopsis, oat, rice, etc. (He et al., 2002; Kim et of metabolites during senescence (Cano-Delgado et al., 2004; Wang and
al., 2009; Kong et al., 2006; Shan et al., 2011; Ueda and Kato, 1980). Chory, 2006; Yang et al., 2011). However, the molecular mechanism of
Exogenous application of MeJA causes increased expression of SAGs BR action on leaf senescence is not fully known yet (He et al., 2001; Lim
such as SEN4, SEN5, and -VPE and loss of chlorophyll content and pho- et al., 2007). The effects of exogenous application of BRs (5 M) on se-
tochemical efciency in Arabidopsis. Mutant studies have further con- nescence were assessed in jujube fruit (Zhu et al., 2010). BRs effectively
rmed the role of JA in leaf senescence as JA-induced senescence is enhanced the activities of superoxide dismutase (SOD), phenylalanine
absent in the JA-insensitive mutant coronatine insensitive 1 (coi1) ammonia-lyase, polyphenoloxidase as well as catalase and delayed
(Shan et al., 2011; Xiao et al., 2004). JA shows its role in leaf senescence fruit senescence and maintained fruit quality by reducing ethylene pro-
by repressing the protein rubisco activase (RCA), and this repression is duction (Zhu et al., 2010). A few years ago, Salam-a (2007) found
coil dependent. The genetic and physiological studies show that this re- that exogenous application of epibrassinolide (eBL) at 10 and 0.1 M
pression of RCA associated with JA-regulated leaf senescence, and that accelerated leaf senescence in wheat plants due to increased peroxidase
loss of RCA causes general senescence-linked characteristics (Shan et activity and decreased protease activity and chlorophyll contents
al., 2011). The JA-induced leaf senescence was further elaborated by (Salam-a, 2007). However, in contrast, it has also been observed
the observation of OsDOS) gene, which is a negative regulator for leaf that BRs are also involved in delaying leaf senescence by improving
senescence (Kong et al., 2006; Lim et al., 2007). Studies on the OsDOS chlorophyll pigments. Chlorophyll breakdown is one of the vital indica-
overexpressing plants and RNAi knockdown plants have revealed that tors for the measurement of leaf senescence and BRs are reported to be
many of the JA signalling-dependent genes were up-regulated in the involved in adversely affecting the photosynthetic apparatus of plant
RNAi transgenic lines but down-regulated in the over-expressing trans- organs (Rao et al., 2002; Salam-a, 2007; Vardhini and Rao, 2002).
genic lines (Shan et al., 2011). These observations validate the As there is no much information available in the literature on the role
co-regulation of JA signalling pathway with senescence. of BRs in leaf senescence so the mechanism how BRs regulate leaf senes-
cence is not fully known.
5.5. Salicylic acid
5.7. Auxins
Although the role of salicylic acid (SA) has been widely studied in
disease resistance, it also shows involvement in leaf senescence Auxins, referred to as generally plant development hormones, play a
(Table 1). Similar to JA the endogenous level of SA is four times higher signicant role in leaf senescence (Kim et al., 2011a; Lim et al., 2007,
in the leaves undergoing senescence (Lim et al., 2003, 2007). 2010; Sexton and Roberts, 1982). Evidence came from up-regulation of
Arabidopsis mutants like npr1 and pad4, defective in SA signalling, ex- some key auxin biosynthetic genes (Van der Graaff et al., 2006), like
hibit reduced expression of a number of SAGs such as PR1a, chitinase, tryptophan synthase (TSA1), IAAld oxidase (AO1), and nitrilases
and SAG12 (Buchanan-Wollaston et al., 2003; Lim et al., 2007; Quirino (NIT1-3), and consequently increased auxin concentration in the
et al., 2000; Rao et al., 2002). Transcriptome proling reveals high senescing leaves. Further, when auxins are applied exogenously they
level of similarities between SA pathway and senescence pathway in are reported to cause down-regulation of some SAGs (Hong et al.,
gene modulation (Van der Graaff et al., 2006). Morris et al. (2000) and 2000; Jones et al., 2010; Kim et al., 2011a; Noh and Amasino, 1999).
Buchanan-Wollaston et al. (2005) also postulated the involvement of Thus, auxins are contemplated as negative regulators of leaf senescence.
SA in the regulation of gene expression during developmental Another interesting observation to note is that auxin concentration
senescence. changes considerably during senescence (Addicott et al., 1955; Ellis et
As SA is also involved in pathogen mediated response and cell death, al., 2005; Lim et al., 2007; Van der Graaff et al., 2006). They cause
its involvement in senescence-associated cell death has been proposed down-regulation of over a half of the genes of auxin transport (Van der
(Coll et al., 2011; Feys et al., 2005). There is an evidence which indicates Graaff et al., 2006) which may result in uneven distribution of auxins.
that SA might be involved in senescence-associated cell death (Coll et Analysis of genetic mutants defective in auxin signalling further rein-
al., 2011; Feys et al., 2005; Rao et al., 2002). The evidence came from forces their role in leaf senescence (Ellis et al., 2005; Lim et al., 2007,
analysis of Arabidopsis pad4 mutants, defective in the SA signalling path- 2010; Okushima et al., 2005). For example, a transcription repressor of
way, also showed impaired cell death (Brosch and Kangasjrvi, 2012; auxin signalling pathway, AUXIN RESPONSE FACTOR 2 (ARF2), is
Yoshimoto et al., 2009). up-regulated during leaf senescence (Ellis et al., 2005; Lim et al., 2010).
1164 M. Sarwat et al. / Biotechnology Advances 31 (2013) 11531171

It has been reported that the T-DNA mutants of ARF2 cause delay in leaf 2010; Serani-Fracassini et al., 1980). Natural PAs are actively in-
senescence, suggesting their role as positive regulators in the process volved in events related to PCD (Kusano et al., 2008). As suppression
(Lim et al., 2007; Xu et al., 2011). YUCCA6, which is a member of avin in the levels of endogenous polyamines has been observed in
monooxygenase family of proteins, catalyses a rate-limiting step in senescing/aging leaves, so it is believed that they have a key role in
auxin biosynthesis (Kim et al., 2011a; Mashiguchi et al., 2011) and controlling leaf senescence (Chen and Kao, 1991). So far it is evident
Arabidopsis plants over-expressing YUCCA6, e.g., the 35S:YUC6 transgen- that PAs are involved in many plant developmental processes such
ic plants and yuc6-1D activation mutant, exhibit high-auxin phenotypes as oral initiation and development, cell division, embryogenesis,
and show markedly increased longevity (Kim et al., 2011a). All these re- root growth, reproductive organ development, tuberization, fruit de-
ports clearly depict the effective role of auxins in regulation of leaf velopment, ripening, and leaf senescence (Galston et al., 1997;
senescence. Nambeesan et al., 2010; Tiburcio et al., 2002).
A number of reports available show the role of PAs in delaying senes-
5.8. Gibberellins cence of leaf, ower as well as fruit (Pandey et al., 2000). For example, in
barley, Sobieszczuk-Nowicka et al. (2009) investigated the changes in
Like other plant hormones, gibberellins also have a signicant im- the levels of PAs bound to thylakoids in senescing leaves and found
pact on leaf senescence (Table 1). As chlorophyll degradation is one of that Put and Spd increased as senescence progressed, whereas Spm de-
the potential indicators of leaf senescence, so effect of any agent on creased. Furthermore, PAs associate with numerous molecules by the
chlorophyll degradation can be directly related to leaf senescence. Chlo- binding action of different types of proteins (Serani-Fracassini and del
rophyll breakdown was considered to be associated with endogenous Duca, 2008). In chloroplasts, covalent binding of PAs to proteins might
gibberellin content in shoots of Paris polyphylla during senescence (Li play a considerable role in the post-translational modications of struc-
et al., 2010; Pandey et al., 2007). Delayed leaf senescence with exoge- tural enzymes/proteins (Dondini et al., 2003; Sobieszczuk-Nowicka et
nous application of gibberellins has been reported in various plant spe- al., 2007, 2008). Transglutaminases (TGases), a protein family, as well
cies. For example, plant species in which GA3 delays senescence include as Pas are involved in reactions leading to senescence/PCD in animals
lettuce (Aharoni and Richmond, 1978), Rumex crispus and R. obtusifolius (Kuehn and Phillips, 2005; Serani-Fracassini and Del Duca, 2008). How-
(Leopold, 1971), Catharanthus roseus (Pandey et al., 2007), nasturtium ever, no information is available on the role of these biomolecules in se-
(Tropaeolum majus) (Beevers, 1966), and Dioscorea rotundata (Ile et nescence as well as PCD in plants (Lorand and Graham, 2003; Seiler and
al., 2006). Raul, 2005).
Recently, a study with perennial plant P. polyphylla (Li et al., 2010) Biogenic, growth-promoting and anti-senescence PAs are key factors
has shown that exogenous application with gibberellic acid (GA3) con- in seed production, fruit ripening and senescence, owering, embryo de-
siderably enhanced the level of internal GAs (GA4 +GA7) resulting in re- velopment, and fruit set (Nambeesan et al., 2008). In different studies, ex-
tardation of shoot senescence, which was attributed primarily to the pression of a yeast SAMdc in tomato indicated that S-adenosylmethionine
suppression of degradation of proteins and chlorophyll as well as (SAM) availability was not limiting for ethylene biosynthesis. The conse-
lipoxygenase activity (Li et al., 2010). A few years ago, it has been con- quences of ripening-specic expression of ySAMdc in tomato include
rmed that both GA and ABA act antagonistically to regulate different de- prolonged vine life, high amount of lycopene and enhanced fruit quality
velopmental processes. This has been revealed after determining (Mattoo and Handa, 2008). In another investigation, expression of yeast
physiological changes taking place in aging leaves associated with senes- spermidine synthase (ySpdSyn) was found to be associated with in-
cence; in particular the changes related to the hormonal and oxidative creased intracellular levels of Spd in the leaf and fruit development
metabolisms have showed that they signicantly hamper senescence (Nambeesan et al., 2010). Overall, senescence in the transgenic plants
of aerial parts and slow the decline of pigments and total soluble was delayed as compared to that in the WT plants. So, it can be suggested
proteins. However, when plants were treated with paclobutrazol that PAs, particularly Spd, are involved in increasing fruit shelf life, prob-
(PCB), an inhibitor of GA-synthesis, concentration of ABA rose while ably by reducing post-harvest decay and senescence (Mehta et al., 2002;
that of GAs declined, resulting in accelerated senescence, indicating an Nambeesan et al., 2010).
antagonistic role of GA and ABA in the leaf senescence of P. polyphylla Overall, of various hormones discussed above, cytokinins receive a
(Yu et al., 2009). In zoysiagrass, seedlings treated with GA3 delayed the maximum attention in relation to their signicant role in leaf senescence.
darkness-induced leaf senescence. The rst genome-wide trial of Cytokinins and auxins are considered as negative regulators of senes-
senescence was carried-out in a species of turfgrass Zoysiagrass (Zoysia cence in plants. In contrast, ethylene and ABA promote leaf senescence.
japonica), during which the expression of genes responsive to staying The afrmative role of JA and MeJA in leaf senescence has been well doc-
green were identied which showed differences between GA3-treated umented in a number of plants. In addition, BRs are involved in delaying
and non-treated plants under dark conditions. Expression of ve genes, leaf senescence. A number of reports available show the role of PAs and
i.e., An (diphthine synthase gene), Met, V-ATPase, SAM and Cry gibberellins in delaying senescence of leaf, ower as well as fruit. Cur-
(Cryptochrome gene), was investigated. Both real-time PCR and rently, efforts are being made to elucidate how far different plant hor-
RT-PCR indicated the differential expression of these genes, which can mones can regulate leaf senescence. Unravelling of mechanism of
be associated with delayed senescence due to GA treatment (Cheng et signal transduction in leaf senescence would provide an insight to con-
al., 2009). However, the effects of gibberellin on natural senescence trol this phenomenon in different plants including crops for attaining
and the relationship between gibberellins and senescence as well as maximum crop production.
their interaction with other plant hormones, are not fully understood.

5.9. Polyamines 6. Stress and senescence

Polyamines (PAs) include spermine (Spm), putrescine (Put), Stresses (both biotic and abiotic) can induce leaf senescence, as re-
spermidine (Spd) and cadaverine (Cad) which are low molecular vealed by the up-regulation of SAGs under these conditions (Ahmad
weight cations synthesized in almost all biological systems including et al., 2011a, 2011b, 2011c; Koyro et al., 2011). Many defense related
plants (Altman et al., 1977; Kaur-Sawhney et al., 2003; Nambeesan et (DR) and pathogenesis related (PR) genes also are up-regulated dur-
al., 2010; Pandey et al., 2000). In general, PAs levels have been ing senescence (Quirino et al., 2000). Genomic studies on A. thaliana
reported to be high in actively growing tissues (Bachrach, 1973; (Gepstein et al., 2003; Guo et al., 2004; Lin and Wu, 2004) and
Galston and Kaur-Sawhney, 1980; Mattoo et al., 2010) and low in P. tremula (Andersson et al., 2004; Bhalerao et al., 2003) further con-
senescing tissues (Altman and Bachrach, 1981; Nambeesan et al., rm the role of DR genes in leaf senescence.
M. Sarwat et al. / Biotechnology Advances 31 (2013) 11531171 1165

6.1. Role of transcription factors in regulation of leaf senescence under analyses show its overlapping role in salt and H2O2 signalling pathways
stress conditions (Balazadeh et al., 2011).
Not only transcription factors and ROS are involved in leaf senes-
There is now a growing body of evidence that stressful conditions/ cence under stress conditions, there are several other metabolites
agents can regulate transcription factors involved in the regulation of which play an active role in causing leaf senescence under stress con-
genes which induce leaf senescence (Breeze et al., 2011; Lee et al., ditions. Thus, the role all such metabolites need to be fully elucidated.
2012; Woo et al., 2010). For example, a recently identied abscisic
acid (ABA)-responsive NAC transcription factor VND-INTERACTING2 7. Micro RNA and senescence
(VNI2) has been reported to negatively regulate leaf senescence
(Yang et al., 2011). VNI2 over-expressing plants show delayed senes- MicroRNAs are single stranded, genome encoded, and small RNA
cence, whereas it is accelerated in a VNI2-decient mutant. VNI2 tran- molecules that regulate key levels of target transcript either by cleav-
scription factor binds to the promoters of the COR (COLD-REGULATED) age or translation suppression (Naqvi et al., 2009, 2012). There are
and RD (RESPONSIVE TO DEHYDRATION) genes. The COR and RD >1000 miRNAs reported from various plants and this list is still in-
over-expressing plants exhibit prolonged leaf longevity (Nakashima creasing day by day. MicroRNAs have been associated with diverse
et al., 2011; Yang et al., 2011). Thus, VNI2 transcription factor provided developmental and physiological processes in plants (Branscheid et
a molecular link which assimilated plant responses to different stresses al., 2010; Naqvi et al., 2010, 2011a, 2011b; Yoon et al., 2010). Howev-
and delays leaf senescence (Yang et al., 2011). Recently, new roles are er, very few reports demonstrate a clear evidence of their role in plant
identied for the acyl-CoA-binding proteins (ACBPs) which are impor- aging. Recently, two independent studies highlight the contribution
tant constituents of phospholipid metabolism (Xiao and Chye, 2011). of at least two miRNAs viz., miR164 and miR319 in regulating plant
These proteins have been reported to modulate plant development aging (Pulido and Laufs, 2010; Schommer et al., 2008). We have
and delay leaf senescence by generating freezing tolerance, oxidative discussed below the role of these miRNAs in senescence.
stress tolerance, heavy metal resistance and pathogen resistance
(Xiao and Chye, 2011). Efforts are currently underway at different in- 7.1. miR164
stitutions to identify specic transcription factors and elucidate their
role in regulation of genes which induce leaf senescence. This advanced Recently, Kim et al. (2009) identied ORE1 gene that is a positive
knowledge will certainly help control leaf senescence. regulator of senescence in Arabidopsis. The ORE1 mutants exhibit de-
layed aging symptoms which include high photochemical activity, re-
duced chlorophyll loss, reduction in dying cells and induction of aging
6.2. Role of reactive oxygen species associated genes, etc. (Kim et al., 2009; Lim et al., 2007; Schippers et
al., 2008). Genetic analysis has shown that the corresponding loci en-
Reactive oxygen species (ROS) are also known to play a signicant code for a NAC2 protein. Previously, it was demonstrated that the ex-
role in stress signalling and senescence (Bhattacharjee, 2005; Jimnez pression of this particular transcript increases with aging (Guo and
et al., 1998; Lee et al., 2011; Lin and Kao, 1998; Munne-Bosch and Gan, 2006; Guo et al., 2004). Being a transcription factor, the NAC2
Alegre, 2002). ROS generation is one of the earliest responses of plant was observed to be localized in nucleus and it probably regulates
cells under abiotic stresses (Ahmad et al., 2008, 2010a) and senescence transcription of various downstream senescence related genes.
(Khanna-Chopra, 2011; Lee et al., 2012). The disturbance in balance be- In plants, majority of transcription factors are known to be under di-
tween production and scavenging of ROS under different environmen- rect control of microRNAs (Rajagopal et al., 2006). Therefore, ORE1 was
tal stresses resulted in increased intracellular ROS levels (Ahmad et al., searched for potential miRNA binding sites on the encoded transcript.
2010a, 2010b, 2011a, 2011b, 2011c; Koyro et al., 2011). ROS are delete- Interestingly, it was found that miR164, an evolutionary conserved
rious to biomolecules, like proteins, lipids, carbohydrates, DNA and ulti- miRNA among plant lineage that regulates CUC/NAC family of transcrip-
mately result in cell death (Ahmad et al., 2008, 2010a, 2010b, 2011a, tion factors, binds to ORE1 (Mishra and Mukherjee, 2007; Zhu et al.,
2011b, 2011c; Koyro et al., 2011). Environmental stresses cause 2012). This was further conrmed that miR164 levels increase with
ROS-linked damage to chloroplasts. A similar scene is observed in aging, an expected pattern exhibited by most of the bonade
normal senescence as ROS-scavenging ability declined on ageing. microRNAtarget pairs (Kim et al., 2009; Pulido and Laufs, 2010).
ROS function by initiation of protein degradation through the pro- MiR164 family, in Arabidopsis, has three different members viz.,
teolytic enzymes cysteine and serine proteases is also evident miR164a, miR164b and miR164c and all of them target CUC/NAC tran-
(Khanna-Chopra, 2011). scription family genes. These genes have well dened roles in leaf mor-
Research on the catalase (a H2O2-scavenging enzyme) throws light phology where they control organ boundary and serration (Nikovics et
on the involvement of H2O2 in leaf senescence. Catalase regulates the al., 2006).
intracellular H2O2 (Ahmad et al., 2008, 2010a, 2010b; Koyro et al., The levels of ORE1 were checked in miR164 triple mutants and in
2011). During leaf senescence CATALASE2 (CAT2) expression is miR164 over-expressing lines of Arabidopsis (Kim et al., 2009). It was
down-regulated and is postulated to be involved in the increase of observed that ORE1 expressed at higher levels in mutants while signif-
H2O2 level (Smykowski et al., 2010). A DNA-binding protein, G-Box icant reduction was noticed in case of miR164 over-expressing lines
Binding Factor1 (GBF1), reported as the CAT2 promoter has further in- (Kim et al., 2009). Similarly, accumulation of ORE1 was noticed in a
creased our knowledge of involvement of CAT2 in senescence transgenic line of Arabidopsis expressing ORE1 resistant to miR164
(Smykowski et al., 2010). At the onset of senescence in gbf1 mutant binding. Taken together, these results clearly suggest that miR164 fam-
plants, the level of CAT2 decreases; H2O2 does not remain at elevated ily members regulate the levels of ORE1 transcripts. Further, miR164 tri-
level and there is delayed expression of SAGs (Miao et al., 2004; ple mutant plants have high levels of ORE1 at early stages of infection
Smykowski et al., 2010). All this clearly indicates the involvement of but no signicant changes were noticed at later stages. This indicated
H2O2 in leaf senescence possibly mediated by GBF1. Another recently that miR164 controls aging at early stages of plant growth. Thus,
identied H2O2 responsive gene is the transcription factor ORS1, a miR164 gene family acts as a negative regulator of plant aging.
paralog of ORE1/ANAC092/AtNAC2, a previously observed regulator Now the question arises as to how miR164 levels decline with aging
of leaf senescence (Balazadeh et al., 2011; Kim et al., 2009). The pro- in plants? To address this, the miR164 levels were analysed in other ORE
moter sequences of both the genes are highly conserved in family mutants. Intriguingly, it was found that miR164 levels remained
Brassicaceae. ORS1, similar to ORE1, is a positive regulator of senescence unchanged in ORE3-1 mutant. The ORE3-1 locus encodes EIN-2 tran-
(Balazadeh et al., 2011; Kjaersgaard et al., 2011). Global expression scription factor which mediates age-dependent down-regulation of
1166 M. Sarwat et al. / Biotechnology Advances 31 (2013) 11531171

miR164 (Chakrabarti, 2010; Kim et al., 2009). Moreover, the ORE1 expression of several genes from leaf morphogenesis to leaf senescence.
mRNA accumulated at high levels in EIN2 mutant. Thus, while EIN2 in- miR164 and miR319 target ORE1 (NAC) and TCP transcription factors,
duces ORE1 transcription, the same TF leads to reduction in miR164 respectively, mediate pathways converging at senescence. However, it
transcript levels. In agreement to this, Arabidopsis mutants for both is still a matter of discussion how miRNAs exhibit coordination in
EIN2 and ORE1 exhibit much delayed expression of senescence related these well diversied levels. An organized approach in studying
genes like SAG12 and consequently delayed loss of Fv/Fm, when com- miRNAs controlling leaf senescence should be the immediate need of
pared with either of the single mutants (Lim et al., 2007) which indicat- the time.
ed that ORE has a denite role in delaying aging. Stress-induced disturbance in balance between accumulation and
scavenging of ROS is believed to result in enhanced intracellular ROS
7.2. miR319 levels, thereby signicantly stimulating the process of senescence.
However, identication and then silencing/expressing defense and
MiR319 is one the earliest miRNAs identied and is highly con- pathogenesis-related genes using advanced molecular techniques
served across the plant kingdom. It has been extensively studied in could be used to delay leaf senescence.
terms of the targets it regulates which include well known transcrip- Hormonal regulation of senescence is very important as it involves
tion factors (TF) TEOSINTE BRANCHED/CYCLOIDEA/PCF (TCP). a complex interplay of signalling molecules at various stages of senes-
MiR319 targets ve different TCP members and any alteration in cence. Global expression proling and availability of genetic mutants
this control leads to leaf deformation, in both Arabidopsis and tomato have unravelled the mystery of these marvellous molecules. Howev-
(Ori et al., 2007; Palatnik et al., 2003). These TCP TFs control the cell er, the exact mechanism how hormones delay or hasten the process
division and thus maintain the leaf morphology. Jasmonic acid (JA) of plant senescence is not yet well known. Therefore, there is still a
is one of the plant hormones that are well recognized in controlling dire need to study the role of hormones in senescence at the physio-
leaf senescence (Schommer et al., 2008; Yun-xia et al., 2010). Several logical and molecular levels. It could be helpful in preventing losses
miRNAs are known to directly target genes involved in biosynthesis/ during the storage of fruits, legumes, owers, and crops. Particularly,
transport of hormones (Lafos et al., 2011). This study provides yet an- by modulating the hormones involved in the senescence pathway,
other, albeit indirect, mode of regulation of miRNA-mediated regula- the shelf-life of these economically important plants can be increased.
tion of plant hormones. The study by Schommer et al. (2008) Therefore, the introgression of genes as well as identication of QTLs
proposes a new role to miR319-targeted TCP TF in leaf senescence related to different hormones synthesis involved directly in the pro-
by affecting the JA biosynthesis. cess of senescence could be further studied. Certainly, future research
In global transcriptome proling, it was noticed that a large num- on leaf senescence will be an amalgamation of bioinformatical predic-
ber of genes were induced in miR319 resistant TCP4 over-expressing tions, hormonal regulation of senescence, miRNA regulations of genes
plants, including those involved in oxylipin biosynthesis (Pulido and and microarray based genetic proling of Arabidopsis mutants that
Laufs, 2010; Schommer et al., 2008). The promoter analysis revealed will unravel the mechanism underlying leaf aging.
that these 8 of the 19 oxylipin biosynthesis pathway genes shared a
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