See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/229183708

Effect of long photoperiod on the reproductive and bulbing processes in garlic

(Allium sativum L.) genotypes

Article  in  Environmental and Experimental Botany · June 2011

DOI: 10.1016/j.envexpbot.2010.11.008

CITATIONS READS

21 1,217

4 authors, including:

Deepu Mathew Haim D Rabinowitch

Kerala Agricultural University Hebrew University of Jerusalem
110 PUBLICATIONS   201 CITATIONS    145 PUBLICATIONS   3,859 CITATIONS   

SEE PROFILE SEE PROFILE

Rina Kamenetsky
Agricultural Research Organization ARO
146 PUBLICATIONS   1,698 CITATIONS   

SEE PROFILE

Some of the authors of this publication are also working on these related projects:

DBT Proect - MARKER ASSISTED BREEDING TO DEVELOP A BACTERIAL WILT RESISTANT CHILLI PAPRIKA VARIETY (Capsicum annuum L.) SUITED FOR THE TROPICAL
REGIONS OF INDIA View project

Planning Board - Finishing School in Biotechnology View project

All content following this page was uploaded by Deepu Mathew on 20 October 2017.

The user has requested enhancement of the downloaded file.

 Environmental and Experimental Botany 71 (2011) 166–173

Contents lists available at ScienceDirect

Environmental and Experimental Botany

journal homepage: www.elsevier.com/locate/envexpbot

Effect of long photoperiod on the reproductive and bulbing processes in garlic

(Allium sativum L.) genotypes
Deepu Mathew a , Yitzhak Forer b , Haim D. Rabinowitch c , Rina Kamenetsky b,∗
a
Department of Horticulture, Krishi Vigyan Kendra, Kerala Agricultural University, Tavanur 679 573, India
b
Department of Ornamental Horticulture, Agricultural Research Organization, The Volcani Centre, 50250 Bet Dagan, Israel
c
The Robert H. Smith Faculty of Agricultural, Food, and Environmental Quality Sciences, The Hebrew University of Jerusalem, 76100 Rehovot, Israel

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

Article history: Garlic (Allium sativum L.) genotypes differ considerably in scape length, flowering ability, and seed pro-
Received 19 January 2010 duction. In bolting clones reproductive processes are facilitated by a combination of specific temperature
Received in revised form and photoperiod regimes. However, it is yet unclear whether the phase-specific photoperiod effect on
22 November 2010
florogenesis is universal for all garlic genotypes. We investigated the effect of ambient day length inter-
Accepted 25 November 2010
ruption by 10 or 30 days of long photoperiod in ten garlic accessions belonging to four bio-morphological
groups. It was evident that garlic genotypes vary significantly in response to long photoperiod, and that in
Keywords:
some clones the treatment enhances florogenesis, flower stalk elongation and bulbing. The competition
Breeding
Development
for resources by the simultaneously developing bulb and inflorescence sinks differentially determines
Diversity the fate of stalk elongation and flower development in the investigated genotypes. It is concluded that
Flowering physiology florogenesis in garlic can be promoted by exposure to proper environmental stimuli, during pre-planting
Genetic variability storage and sprouting to the later growth stages. The genetic variability acquired from sexual reproduc-
Sexual propagation tion and vegetatively preserved collections can serve in genetic and physiological studies as well as in
Seed production breeding programs.
© 2010 Elsevier B.V. All rights reserved.

1. Introduction
Modern garlic cultivars are sterile, and seed production was
reported only for a few genotypes from Central Asia and Cau-
casia (Etoh, 1986; Etoh et al., 1988, 1992; Baitulin et al., 2000;
Simon, 2003; Kamenetsky et al., 2004b, 2005). Limited number
of seeds was obtained in bolting genotypes following continuous
removal of topsets from intact inflorescences (Etoh, 1985; Etoh
et al., 1988; Takagi et al., 1993; Inaba et al., 1995; Jenderek, 1998;
Jenderek and Hannan, 2000, 2004a; Etoh and Simon, 2002), topsets’
removal from detached inflorescences (Pooler and Simon, 1994)
and by hand-pollination (Kononkov, 1953; Novak and Havranek,
1975). Competition among simultaneously developing sinks such
as bulbs and inflorescences (Etoh and Simon, 2002) ovular abor-
tion in fertile plants due to adverse environments (Qu-Ying et al.,
1994), pathogen infection (Konvicka, 1984; Etoh, 1982), mutations,
or genetic male sterility (Oh and Kim, 1992) were proposed as main
reasons for infertility.
Garlic genotypes differ considerably in the degree of scape elon-
gation, and were thus classified as: (1) nonbolters – plants do not
∗ Corresponding author. Tel.: +972 3 968 3511; mobile: +972 50 6220 511.
E-mail addresses: vhrkamen@volcani.agri.gov.il, rmgold@agri.huji.ac.il
(R. Kamenetsky).
normally form a flower stalk; (2) incomplete bolters – plants pro-
duce a thin, short flower stalk with only a few topsets, and usually
form no flowers; and (3) complete bolters – plants produce a long,
thick flower stalk, with flowers and topsets (Takagi, 1990). Previous
findings were restricted to the field evaluation of the reproductive
potential of very few accessions whereas the present study reveals
the physiological variability of accessions with wide bio-geographic
variations in their response enhanced photoperiods.
In geophytes, florogenesis and seed production markedly
depend upon the results of the competition for nutrients with the
simultaneously developing bulbs (Le Nard and De Hertogh, 1993).
In bulb onion, a strong sink at early stages of bulb development
suppresses growth and differentiation of the young inflorescence
with the consequent drying out of the flower stalk (for review,
see: Rabinowitch, 1990). Hence the photoperiod influence on floral
development should be considered in the context of the simulta-
neous but competitive development of storage and reproductive
organs.
A study of temperature and photoperiod effect on garlic growth
and florogenesis provided an insight to the enigma of garlic sterility
and offered environmental tools for flowering regulation and fer-
tility restoration (Kamenetsky et al., 2004a). Long photoperiod [LP]
triggers the initial elongation of flower stalks within the developing
garlic bulbs, but exposure to extended periods of LP results in inter-
ference of flower development by differentiation and growth of

0098-8472/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.envexpbot.2010.11.008
 D. Mathew et al. / Environmental and Experimental Botany 71 (2011) 166–173
topsets (Kamenetsky et al., 2004a). Photoperiod, like other environ-
mental stimuli, regulates plant response through internal signals
and changes in hormones profile. LP is known to enhance endoge-
nous gibberellins’ levels, with the consequent florogenesis (King
et al., 2006).
Mutations during millennia of garlic vegetative propagation
resulted in high heterogeneity and increased genotypic and pheno-
typic variability between the clonally propagated cultivars (Simon
and Jenderek, 2003). However, our experiments with phase-
specific application of photoperiod resulted in flowering and seed
production in a few garlic accessions (Kamenetsky et al., 2004a). It
is yet unclear whether phase-specific LP effect on garlic florogen-
esis and seed production is universal, and the extent of variability
requires investigation of genotype × environment interactions.
In this study, the effect of phase specific LP on florogenesis,
flower stalk elongation, and bulbing in ten accessions from different
sources was investigated. We hypothesized that long photoperiod
enhances both florogenesis and bulbing, and that the genotypes
differ in photoperiod requirements for these developmental pro-
cesses. Thus, under specific growth conditions, the competition
from the simultaneously developing sinks will differentially deter-
mine the fate of stalk elongation and flower development in the
tested genotypes.
2. Materials and methods
All experiments were performed at the Institute of Plant Science,
The Volcani Centre, Israel. Scanning electron microscopy (SEM) was
performed at Robert H. Smith Faculty of Agriculture, Food and Envi-
ronment, The Hebrew University of Jerusalem, Rehovot, Israel.
2.1. Experimental material
Ten garlic (Allium sativum L.) clones from different climatic
regions (Supplemental Table 1) were obtained from the Field
Gene Bank for Vegetatively Propagated Short-Day Allium spp. in
Israel. The specific genotypes were selected upon their morpho-
physiological traits and bolting habit under Israeli conditions, thus
classified as (1) non-bolting, (2) semi-bolting, (3) bolting with
mainly topsets and (4) bolting with mainly flowers in the inflo-
rescence (Supplemental Table 1).
Sixty uniform cloves per accession, free of bruises or infec-
tions, were randomly selected, sorted, cleaned and treated with
0.2% Benlate (Du Pont De Nemours, France) and 1% Marpan 50WP
(Machteshim, Israel). Following a 8 weeks cold treatment at 4 ◦ C
(65–70% RH), cloves were planted on November 11, 2007, in per-
Fig. 1. Experimental layout and time of plant sampling. Cloves were planted on November 11, 2007 and harvested on June 2, 2008. LP, long photoperiod; DAP, days after
planting.
167
forated plastic trays containing 70% 0.8 mm volcanic tuff particles
(Israel, Golan Heights), 20% perlite and 10% ground coconut peels.
The growing trays were placed in an insect proof 50 mesh net-house
providing 30% shade, and fertigated regularly with “Shefer” liquid
fertilizer (N:P:K = 59:35:94 g L−1 , Dshanim, Israel). Standard control
of pathogens was applied throughout.
2.2. Experimental layout and monitoring developmental
parameters
Ambient photoperiod and maximum and minimum tempera-
tures at Bet-Dagan, Israel, during the period of study are presented
in Supplemental Fig. 1a and b.
Control plants were grown under natural photoperiod through-
out. On the 79th day after planting (DAP), 20 plants per accession
were exposed to 10 or 30 days long photoperiod (LP) interruption
(Fig. 1). LP consisted of 8.5 h natural day light followed by 9.5 h of
incandescent light (4 ␮mol m−2 s−1 PAR). Timer controlled the roll
down of shutters (Galcon, Israel) separating between photoperiod
treatments.
Experimental layout and sampling times are presented in Fig. 1.
Randomly selected 3–5 plants of each accession from all treat-
ments were dissected and studied on the 87, 99, 120 and 142 days
after planting. Shoot apical meristem (SAM), flower stalk length
and number of flowers in the inflorescence were examined under a
stereoscope (Stemi 2000-C, Zeiss, Germany). For scanning electron
microscopy (SEM) studies, freshly harvested plants were care-
fully stripped of their leaves and spathes. Meristems were fixed
in a 5:5:90 mixture of glacial acetic-acid:formalin (40%):ethanol
(70%), dehydrated in a graded ethanol series (25, 50, 75, 95, and
100%), dried using liquid CO2 in a Bio-Rad 750 critical-point dryer,
mounted on SEM stubs and gold coated. Images were obtained
directly from the SEM (JSM-35C, JEOL Japan) at 15 kV (Kamenetsky,
1994).
2.3. Data analysis
A randomized blocks’ design was applied to the greenhouse
experiment, three blocks per treatment of normal, 10 and 30 days
LP conditions. Within each block, 10 accessions were randomly
arranged. The significance of treatment effects was analyzed by
one-way ANOVA using the JMP statistical software (SAS Institute,
Version 7.0). The means over the three replications were compared
using the Tukey’s post-ANOVA test (Tukey, 1949). Stalks’ lengths
were measured on 99, 120 and 142 DAP, and statistical signifi-
cance of the differences in each accession was analyzed for each
168 D. Mathew et al. / Environmental and Experimental Botany 71 (2011) 166–173
Fig. 2. Effect of naturally increasing day length, and 10 or 30 days 16 h LP interruption on flower stalk length (cm) and bulb weight (g) in the non-bolter #2272 and semi-bolter
‘Shani’. Records were taken on the 142nd DAP.
sampling date separately. Similarly, the treatment effects on final
bulbs’ weight on the 142nd DAP day and the number of flowers
and topsets on the 170th DAP were analyzed for each accession.
The data shown are mean values ± standard error (SE).
3. Results
3.1. Variability in floral initiation and initial stalk elongation
under naturally increasing photoperiod
The ten studied garlic accessions varied considerably both, in
the physiological age (number of leaves) and in the time of tran-
sition from the vegetative to the reproductive stage, irrespective
of their bio-morphological classification and origin (Supplemental
Table 1 and Fig. 2). The apical meristem of the non-bolting accession
#2272 remained vegetative throughout, and its plants produced
up to 17 leaves prior to bulbing and maturation. The semi-bolting
‘Shani’ and the bolting accessions #2684, #2525 and #2212 were
the earliest, and the topset-producing accession #2509 was the lat-
est to initiate reproductive meristems (Supplemental Table 1). The
difference for floral transition between the earliest and latest geno-
types was up to 40–50 days, and the number of leaves ranged from
9 to 16.
The variation in time to floral transition remained evident in the
later stages of flower differentiation. Hence, on 87 DAP the apical
meristem of #2509 was vegetative, while that of #2525 has almost
completed its differentiation and numerous flowers were visible
(Supplemental Fig. 2).
3.2. Effect of long photoperiod on floral stalk elongation
The effect of the natural photoperiod interruption by 10 or 30
days 16 h LP on flower stalk elongation was measured on the 99th
and 142nd DAP (equal to 20 and 43 days after the beginning of LP
treatment, respectively). On the first reading, stalk elongation was
evident only in two accessions. In #2359, 10 days LP resulted in
up to 25 cm long stalks, as compared with 5–7 cm under natural
photoperiod (day length increased from ∼10 to 10.5 h). Similarly,
in both 10 days and 30 days LP treatments, scapes of #3028 reached
20 cm long, as compared with 2–3 cm in the control plants. At this
time, scapes’ length of the other tested genotypes was equal to
control (data not shown).
On the 142nd DAP, flower stalks reached their final lengths
in the 8 bolting genotypes, but no effect was evident in the non-
bolting accession #2272, and the semi-bolting ‘Shani’. The former
remained vegetative, and the latter had a 30 cm long scape as in
control under ambient conditions (Fig. 2).
In bolting genotypes, stalk elongation was differentially affected
by LP (Fig. 3). Some clones (i.e., #2085, #2684, and #3028)
responded favorably to the two LP treatments, others benefited
from 10 days LP, but stalk growth was suppressed when exposed
to 30 LP (i.e., #2509, #3026, #2085 and #2212).
Taken together, it is evident that 30 days LP resulted in a mixed
response: a retarding effect on scape elongation in four accessions
and promotion of stalk elongation in accessions #3028 and #2525
(Supplemental Fig. 3), thus indicating that final scape length is
determined by the interaction between genotype and environment.
3.3. Effect of long photoperiod on inflorescence development
The non-bolting #2272 and the semi-bolting ‘Shani’ were
excluded from this study. With the exception of the intermediate
type #3026, interruptions of 10 or 30 days LP had no visible effect
on the inflorescence structure of topsets’ producing accessions,
thus no inflorescences had viable flowers at anthesis (Supplemental
Table 1 and Fig. 4). In contrast, LP interruption of the naturally
increasing day length resulted in a significant increase in the
number of flowers per umbel in three out of the four flowering
accessions, as compared with control (Fig. 4 and Supplemental
Table 2), and anthesis in accession #3028 was earlier than con-
trol (Fig. 4). Similar response was evident in plants of #2085 at 10
days LP, but 30 days LP interruption resulted in a complete arrest of
scape elongation and early abortion of the developing inflorescence
buds.
Under naturally increasing photoperiod, inflorescence of acces-
sions #2212 and #2525 produced both flowers and leafy bracts
(Fig. 4). However, the two LP interruption treatments resulted
in increase in both, number and length of green leafy bracts in
the inflorescence and in smaller number of flowers (Supplemental
Table 2 and Fig. 4). Production of topsets and complete suppression
of flower development in #2212, were also evident.
3.4. Effect of long photoperiod on bulb formation
The effect of LP on garlic bulbing was genotype specific
(Figs. 2 and 3). Plants of the non-flowering accession #2272 pro-
duced bulbs irrespective of the photoperiod treatment. A 30 days
LP resulted in a significantly smaller bulb size in both, the semi-
bolting ‘Shani’ and the bolting genotype #2509 than in control and
following 10 days LP interruption (Supplemental Table 3). Under
NP, bulbing of the two flowering accessions #2085 and #2212 was
later than in plants exposed to LP interruptions (Fig. 3).
Throughout, ‘Shani’ and accessions #3028, #2509, and #2525
had a positive correlation between the cumulated mass of floral
stalks and bulbs (r = 0.8057**, 0.65**, 0.566** and 0.50**, respec-
tively). Similar trend was measured for other genotypes, and under
no circumstances a negative correlation among between these
characters was observed.
 D. Mathew et al. / Environmental and Experimental Botany 71 (2011) 166–173 169

Fig. 3. Effect of naturally increasing day length, and 10 or 30 days 16 h LP interruption on flower stalk length (cm) and bulb weight (g) in eight bolting accessions. Records
were taken on the 142nd DAP.
170 D. Mathew et al. / Environmental and Experimental Botany 71 (2011) 166–173
Fig. 4. Effect of NP and interruption by either 10 days or 30 days 16 h LP on inflorescence development in eight bolting genotypes. Note the absence of inflorescence in
accessions #2509, #3026 and #2085 under 30 days LP.
4. Discussion
All commercially grown garlic varieties are sterile and thus
propagated vegetatively. Millennia of mutations and selections
resulted in marked variation between clones in developmental,
horticultural and quality traits (Astley et al., 1982; Hwang, 1993;
Messiaen et al., 1993; Kamenetsky et al., 2005), in physiology
(Pooler and Simon, 1993a; Lallemand et al., 1997), and in molec-
ular characteristics (Etoh et al., 2001; Hong et al., 2000; Volk
et al., 2004; Vieira and Nodari, 2007). Even a greater variation
was recorded among offspring of seedlings populations from fer-
tile garlic plants (Jenderek and Hannan, 2003, 2004b; Jenderek,
2004; Jenderek and Zewdie, 2005; Shemesh et al., 2008). Varia-
tion among garlic genotypes both in florogenesis processes and
in response to environment signals is expected, and is probably
similar to that common in other Allium plants (Rabinowitch, 1985,
1990; Kamenetsky and Rabinowitch, 2002; Khokhar et al., 2007;
Brewster, 2008). However, to the best of our knowledge, informa-
tion on variation in flowering physiology within A. sativum has not
been reported.
4.1. Flowering variability in A. sativum
In this study, garlic genotypes of four bio-morphological groups
varied in response to low storage temperatures and photope-
riod treatments. Microscopic studies of the cold treated plants
showed floral initiation in nine out of the 10 studied genotypes.
No meristem transition was observed in non-bolting accession
#2272, possibly due to the lack insufficient signal strength under
Israeli conditions (Le Nard and De Hertogh, 1993; Flaishman and
Kamenetsky, 2006), degeneration-like diseases (Konvicka, 1984),
or chromosomal aberrations (Etoh, 1985).
Bolting genotypes varied greatly in the number of days from
planting to meristems’ transition and to the initial elonga-
tion of flower stalks (Supplemental Table 1). Large genotypic
variation in response to low temperatures is known in many alli-
aceous crops, including bulb onion (Rabinowitch, 1985, 1990),
shallot (Rabinowitch and Kamenetsky, 2002), and Japanese
bunching onion (Inden and Asahira, 1990), where selection
for genotypes with high and low sensitivity to low temper-
atures and specific response to photoperiod facilitated the
 D. Mathew et al. / Environmental and Experimental Botany 71 (2011) 166–173
wide spread of the crops from the tropics to the temperate
zones.
The studied garlic genotypes from Central Asia belong to the
Longicuspis group (Fritsch and Friesen, 2002; Kamenetsky et al.,
2005). In these bolting plants (e.g., clones #3028 and #2525 in
this study, Supplemental Table 1) florogenesis is controlled by a
cascade of genetic factors that code for the upstream progression
of the process and is differentially regulated by day length and
temperature. Hence, an intimate knowledge of the genetic by envi-
ronment interactions is expected to facilitate fertility restoration in
different genotypes. Fertility restoration and sexual hybridization
are expected to further extend the genetic variability (Shemesh
et al., 2008) and consequently contribute to improved yields and
quality, earliness and lateness, and facilitate the spread of this veg-
etable/condiment beyond the current boundaries.
Genetic variation in both, physiological age and time to floral ini-
tiation is common in many geophytes. Exploitation of this variation
together with horticultural manipulations (forcing, photoperiod
control, planting date, plant density, fertigation, etc.) facilitates the
regulation of both length of the flowering season and its timing,
thus enables a continuous supply of ornamentals year round (Le
Nard and De Hertogh, 1993; Benschop et al., 2010), as well as nick-
ing of parental lines for hybrid seed production (e.g., bulb onion:
Jones and Mann, 1963; Rabinowitch, 1985, 1990; Brewster, 2008).
It is reasonable to assume that advanced understanding of garlic
florogenesis and fertility restoration will result in a major shift from
vegetative to seed propagation (Kamenetsky, 2007). Then, similar
to bulb onion (Jones and Mann, 1963; Rabinowitch, 1985, 1990),
growers of garlic bulbs and producers of seed will face the issue
of bolting control. In the bulb production season, retardation of
bolting contributes to the improvement in quality yield, whereas
maximum flowering in the second season is required for seed pro-
duction with minimum genetic shift and nicking between parental
lines is essential for hybrid seed production. The large variability
in both genetic background and response to environment clearly
shows potential flexibility for future bred cultivars for the improve-
ment of the production chain.
4.2. Effect of LP on garlic florogenesis and bulb formation
In alliaceous crops and in many ornamental bulbs, floral
induction depends upon environment signals, i.e., high (tulip, nar-
cissus) or low (onion) temperatures, or long photoperiod (lily)
(Rabinowitch, 1990; Kamenetsky and Rabinowitch, 2002; Khokhar
et al., 2007; Benschop et al., 2010). Garlic produces poor bulbs in
the warm, short-day lowland tropical regions, but in the temperate
zones, where days are longer and winters are cold, flower induction
and differentiation occur and is often followed by scape elonga-
tion (Brewster, 2008). However, only rarely anthesis comes about,
probably due to endogenous competition for assimilates between
the developing bulb and inflorescence (Rosen and Tong, 2001). Ear-
lier, under controlled photoperiod conditions (Kamenetsky et al.,
2004a), and in the current experiment, we have shown that follow-
ing storage at low temperatures, floral initiation in semi-bolting
and bolting garlic genotypes is induced under short photoperiod
of 10–10.5 h, while scape elongation was strongly affected by long
photoperiod (Fig. 3).
For garlic (Koul and Gohil, 1970; Novak and Havranek, 1975;
Katharzin and Katharzin, 1978, 1982; Koul et al., 1979; Konvicka,
1984; Pooler and Simon, 1994), bulb onion (Brewster, 1990, 2008;
Rabinowitch, 1985, 1990), shallot (Krontal et al., 2000) and other
bulbous geophytes (Le Nard and De Hertogh, 1993) it was sug-
gested that under LP the phenology and final development of plants
depend upon the results of the competition between the storage
bulb and the developing inflorescence for assimilates. When the
171
two competitive processes occur simultaneously, both vegetative
and reproductive organs suffer from insufficient supply of assim-
ilates with the consequent poor yield and quality of bulbs and/or
seed production (Jones and Mann, 1963; Brewster, 1990; Le Nard
and De Hertogh, 1993; Pooler and Simon, 1994), whereas early bul-
bing prohibits scape elongation and further development of the
reproductive organs (Rabinowitch, 1985, 1990).
In the current study, however, we were unable to support the
above assumptions, as flower stalk elongation in garlic had no
adverse affects on bulbs’ weight. We assume that under optimal
growth conditions, bolting in the vegetatively propagated garlic has
only insignificant effect on bulbing and yield. It seems that compe-
tition for resources’ allocation is quite an important factor, but only
as a second or third step downstream a cascade of events.
In three (‘Shani’, #2509, and #3026) genotypes, exposure to LP
resulted in smaller bulbs than those developed under naturally
increasing day length, due to accelerated bulbing and early mat-
uration. These results are in agreement with Mann’s (1952, 1958)
findings on the development of smaller garlic bulbs under con-
tinuous LP regime, and in bulb onion under high temperatures or
extra long photoperiod (Brewster, 1990, 2008). In addition, 30 days
of LP interruption completely arrested stalk elongation in three
accessions (#2509, #3026 and #2085), probably because of early
bulbs’ maturation. Thus, the multifaceted effect of LP on bulbing and
scape elongation provides an insight into regulation, competition
for assimilates and finally resources’ allocation between the simul-
taneously developing two major sinks in garlic plant. In the future,
we plan to study the effect of growth temperature and photoperiod
on bulb dormancy and storage life.
4.3. Effect of LP on flower and topset differentiation
Initially, most bolting garlic genotypes plants differenti-
ate flower buds, which abort at early developmental stages
(Kamenetsky and Rabinowitch, 2001). A continuous removal of
topsets resulted in flowering and seed production (Pooler and
Simon, 1994; Jenderek and Hannan, 2000; Etoh and Simon, 2002).
Millennia of selections by man for the production of early devel-
opment of strong sinks and big bulbs were assumed to result in
endogenous hormonal balance modification in favor of bulbing
(including topsets) (Etoh and Simon, 2002). Our results show that in
garlic plants, this balance is strongly affected by LP, but significant
genotypic effect is clearly evident (Supplemental Table 2). Pooler
and Simon (1993b) suggested that LP reduced the flowering in four
garlic clones. Our work further reveals the physiological and devel-
opmental effects of photoperiod from the vegetative stage through
the completion of florogenesis, as well as variability in response
to the photoperiod available in a highly diverse bio-geographic
germplasm. Earlier, we have shown that environmental signals
are involved in regulation of the differentiation of garlic inflores-
cence with the consequent production of flower and/or topsets in
the inflorescence (Kamenetsky et al., 2004a; Mathew et al., 2005).
Similar response in the reproductive strategy of plants is known
in Titanotrichum oldhamii (Wang and Cronk, 2003) and in Allium
vineale (Davis and Peters, 1964; Ceplitis, 2001). It is interesting
to note that under naturally increasing day length (ca. 12.5–13 h)
plants of #3026 produced both flowers and topsets, while a short
LP interruption resulted in topsets only, and a longer interruption
resulted in inflorescence abortion and earlier bulb formation. Alto-
gether these findings suggest that #3026 genotype is rather early,
namely, bulbing is induced by a relatively short LP common in Israel
in the early spring, and long exposure to LP strongly enhances bul-
bing and maturation on the expenses of the reproductive organs,
as in bulb onion (Kedar et al., 1975; Brewster, 1990, 2008).
Our results indicate that many garlic genotypes may be forced to
flower by exposure to proper environment conditions, from storage
172 D. Mathew et al. / Environmental and Experimental Botany 71 (2011) 166–173
and sprouting to the later growth stages. A successful restoration of
fertility is expected to extend the genetic variability, for utilization
in genetic and physiological studies as well as in breeding programs.
Acknowledgements
DM thanks the Ministry of Human Resource Development, Gov-
ernment of India, for his selection and Ministry of Foreign Affairs,
Government of Israel, for awarding the Israel Government Scholar-
ship 2007–2008, leading to this work.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at doi:10.1016/j.envexpbot.2010.11.008.
References
Astley, D., Innes, N.L., van der Meer, Q.P., 1982. Genetic Resources of Allium species:
A Global Report. International Bureau of Plant Genetic Resources, Rome.
Baitulin, I.O., Agafonova, G., Rabinowitch, H.D., Kamenetsky, R., 2000. Creation of
gene bank of Central Asian species of the genus Allium L., their biology and eco-
nomic potential. In: Granovsky, E.I., Fain, E.E. (Eds.), State and Perspectives of
Scientific collaboration Kazakhstan-Israel. Almaty, Kazakhstan, pp. 87–94 (in
Russian).
Benschop, M., Kamenetsky, R., Le Nard, M., Okubo, H., De Hertogh, A., 2010. The
global flower bulb industry: production, utilization, and research. Hortic. Rev.
36, 1–115.
Brewster, J.L., 1990. Physiology of crop growth and bulbing. In: Rabinowitch, H.D.,
Brewster, J.L. (Eds.), Onions and Allied Crops, vol. I. Botany, Physiology, and
Genetics. CRC Press, Boca Raton, Florida, pp. 53–88.
Brewster, J.L., 2008. Onions and Other Vegetable Alliums, 2nd edition. CAB Interna-
tional, Wallingford, UK, p. 432.
Ceplitis, A., 2001. The importance of sexual and asexual reproduction in the recent
evolution of Allium vineale. Evolution 55, 1581–1591.
Davis, F.S., Peters, E.J., 1964. Reproductive cycles of wild garlic and nomenclature of
plant and bulb types. Weeds 13, 84–87.
Etoh, T., 1982. Development and degeneration of tapetum in garlic (Allium sativum
L.). Mem. Fac. Agric. Kagoshima Univ. 18, 75–84.
Etoh, T., 1985. Studies on sterility in garlic. Mem. Fac. Agric. Kagoshima Univ. 21,
77–132.
Etoh, T., 1986. Fertility of the garlic clones collected in Soviet central Asia. J. Jpn. Soc.
Hortic. Sci. 55, 312–319.
Etoh, T., Simon, P.W., 2002. Diversity, fertility and seed production in garlic. In:
Rabinowitch, H.D., Currah, L. (Eds.), Allium Crop Science: Recent Advances. CAB
International, Wallingford, Oxon, pp. 101–117.
Etoh, T., Noma, Y., Nishitarumizu, Y., Wakamoto, T., 1988. Seed productivity and
germinability of various garlic clones collected in Soviet central Asia. Mem. Fac.
Agric. Kagoshima Univ. 24, 129–139.
Etoh, T., Johjima, J., Matsuzoe, N., 1992. Fertile garlic clones collected in Caucasia.
In: Hanelt, P., Hammer, K., Knupffer, H. (Eds.), The Genus Allium: Taxonomic
Problems and Genetic Resources. JPK, Gatersleben, Germany, pp. 49–54.
Etoh, T., Watanabe, H., Iwai, S., 2001. RAPD variation of garlic clones in the centre
of origin and the western most area of distribution. Mem. Fac. Agric. Kagoshima
Univ. 37, 21–27.
Flaishman, M., Kamenetsky, R., 2006. Florogenesis in flower bulbs: classical and
molecular approaches. In: Teixeira da Silva, J.A. (Ed.), Floriculture, Ornamental
and Plant Biotechnology, vol. I. Global Science Books, Japan, pp. 33–43.
Fritsch, R.M., Friesen, N., 2002. Evolution, domestication and taxonomy. In: Rabi-
nowitch, D., Currah, L. (Eds.), Allium Crop Science: Recent Advances. CAB
International, Wallingford, pp. 5–30.
Hong, C.-J., Watanabe, H., Etoh, T., Iwai, S., 2000. A search of pollen fertile clones in
Iberian garlic by RAPD markers. Mem. Fac. Agric. Kagoshima Univ. 36, 11–16.
Hwang, J.M., 1993. Genetic divergence and classification of garlic cultivars by mul-
tivariate analysis. J. Korean Soc. Hortic. Sci. 34, 257–264 (in Korean).
Inaba, A.T., Ujiie, T., Etoh, T., 1995. Seed productivity and germinability in garlic.
Breeding Sci. 45 (Suppl. 2), 310 (in Japanese).
Inden, H., Asahira, T., 1990. Japanese bunching onion (Allium fistulosum L.). In: Brew-
ster, J.L., Rabinowitch, H.D. (Eds.), Onions and Allied Crops, Biochemistry, Food
Science, and Minor Crops, vol. III. CRC Press, Boca Raton, Florida, pp. 159–178.
Jenderek, M.M., 1998. Generative reproduction of garlic (Allium sativum L.). Zeszyty
Naukowe Akademii Rolniczej im. H. Kollataja w Krakowie 57, 141–145 (in Pol-
ish).
Jenderek, M.M., 2004. Development of S1 families in garlic. Acta Hortic. 637,
203–205.
Jenderek, M.M., Hannan, R.M., 2000. Seed producing ability of garlic (Allium sativum)
clones from two public US collections. In: Proceedings of the 3rd International
Symposium on Edible Alliaceae , 29 October–3 November. University of Georgia,
Athens, Georgia, USA, pp. 73–75.
Jenderek, M.M., Hannan, R.M., 2003. Phenotypic characteristics of open pollinated
garlic progenies. HortScience 38, 673.
Jenderek, M.M., Hannan, R.M., 2004a. Variation in reproductive characteristics and
seed production in the USDA garlic germplasm collection. HortScience 39,
485–488.
Jenderek, M.M., Hannan, R.M., 2004b. Tolerance to rust (Puccinia allii) in seed derived
garlic progenies. HortScience 39, 775.
Jenderek, M.M., Zewdie, Y., 2005. Within- and between-family variability for
important bulb and plant traits among sexually derived progenies of garlic.
HortScience 40, 1234–1236.
Jones, H.A., Mann, L.K., 1963. Onions and Their Allies – Botany, Cultivation, and
Utilization. InterScience Publishers, New York, p. 286.
Kamenetsky, R., 1994. Life cycle, flower initiation and propagation of the desert
geophyte Allium rothii. Int. J. Plant Sci. 155, 597–605.
Kamenetsky, R., 2007. Garlic: botany and horticulture. Hortic. Rev. 33, 123–172.
Kamenetsky, R., Rabinowitch, H.D., 2001. Floral development in bolting garlic. Sex.
Plant Reprod. 13, 235–241.
Kamenetsky, R., Rabinowitch, H.D., 2002. Florogenesis. In: Rabinowitch, H.D., Currah,
L. (Eds.), Allium Crop Science: Recent Advances. CAB International, Wallingford,
Oxon, pp. 31–57.
Kamenetsky, R., Shafir, I.L., Zemah, H., Barzilay, M., Rabinowitch, H.D., 2004a. Envi-
ronmental control of garlic growth and florogenesis. J. Am. Soc. Hortic. Sci. 129,
144–151.
Kamenetsky, R., Shafir, I.L., Baizerman, M., Khassanov, F., Kik, C., Rabinowitch, H.D.,
2004b. Garlic (Allium sativum L.) and its wild relatives from Central Asia: evalu-
ation of fertility potential. Acta Hortic. 637, 83–91.
Kamenetsky, R., Shafir, I.L., Khassanov, F., Kik, C., Van Heusden, A.W., Ginkel, M.V.,
Burger-Meijer, K., Auger, J., Arnault, I., Rabinowitch, H.D., 2005. Diversity in fer-
tility potential and organosulphur compounds among garlics from central Asia.
Biodivers. Conserv. 14, 281–295.
Katharzin, M.S., Katharzin, I.M., 1978. Experiments on the sexual reproduction of gar-
lic. Byulletin’ Vsesoyuznogo Ordena Lenina I Ordena Druzhby Norodov Instituta
Rastenievodstva Imeni N. I. Vavilova 80, 74–76 (in Russian).
Katharzin, M.S., Katharzin, I.M., 1982. On generative reproduction of garlic. Trudy
po Prikladnoi Botanike, Genetike I Selektsii 72, 135–136 (in Russian).
Kedar, N., Levy, D., Goldschmidt, E.E., 1975. Photoperiodic regulation of bulbing
and maturation of Bet Alpha onion (Allium cepa L.) under decreasing daylength
conditions. J. Hortic. Sci. 50, 373–380.
Khokhar, K.M., Hadley, P., Pearson, S., 2007. Effect of photoperiod and temperature
on inflorescence appearance and subsequent development towards flowering
in onion raised from sets. Sci. Hortic. 112, 9–15.
King, R.W., Moritz, T., Evans, L.T., Martin, J., Andersen, C.H., Blundell, C., Kardailsky,
I., Chandler, P.M., 2006. Regulation of flowering in the long-day grass Lolium
temulentum by gibberellins and the FLOWERING LOCUS T gene. Plant Physiol.
141, 498–507.
Kononkov, P.F., 1953. The question of obtaining garlic seed. Sad i Ogorod 8, 38–40
(in Russian).
Konvicka, O., 1984. Generative Reproduktion von Knoblauch (Allium sativum). Allium
Newsl. 1, 28–37 (in German).
Koul, A.K., Gohil, R.N., 1970. Causes averting sexual reproduction in Allium sativum
Linn. Cytologia 35, 197–202.
Koul, A.K., Gohil, R.N., Langer, A., 1979. Prospects of breeding improved garlic in the
light of its genetic and breeding systems. Euphytica 28, 457–464.
Krontal, Y., Kamenetsky, R., Rabinowitch, H.D., 2000. Flowering physiology and some
vegetative traits of short-day shallot–a comparison with bulb onion. J. Hortic.
Sci. Biotechnol. 75, 35–41.
Lallemand, J., Messiaen, C.M., Briand, F., Etoh, T., 1997. Delimitation of varietal groups
in garlic (Allium sativum L.) by morphological, physiological and biochemical
characters. Acta Hortic. 433, 123–132.
Le Nard, M., De Hertogh, A.A., 1993. Bulb growth and development and flowering. In:
De Hertogh, A.A., Le Nard, M. (Eds.), The Physiology of Flowering Bulbs. Elsevier,
Amsterdam, pp. 29–44.
Mann, L.K., 1952. Anatomy of the garlic bulb and factors affecting bulb development.
Hilgardia 21, 195–251.
Mann, L.K., 1958. Growth and bulbing of garlic (Allium sativum L.) in response to
storage temperature of planting stocks, day length and planting date. Hilgardia
27, 384–419.
Mathew, D., Ahmed, Z., Singh, N., 2005. Formulation of flowering index, morpho-
logical relationships and yield prediction system in true garlic aerial seed bulbil
production. HortScience 40, 2036–2039.
Messiaen, C.M., Cohat, J., Leroux, J.P., Pichon, M., Beyries, A., 1993. Les Allium Ali-
mentaires Reproduits Par Voie Vegetative. INRA Publication, Paris.
Novak, F.J., Havranek, P., 1975. Attempts to overcome sterility of common garlic
(Allium sativum). Biol. Plant. (Praha) 17, 376–379.
Oh, D.-G., Kim, K.T., 1992. Search for the fertile garlic clones and the performance of
the hybrids between fertile clones. HortScience 27, 611.
Pooler, M.R., Simon, P.W., 1993a. Characterization and classification of isozyme and
morphological variation in a diverse collection of garlic clones. Euphytica 68,
121–130.
Pooler, M.R., Simon, P.W., 1993b. Garlic flowering in response to clone, photoperiod,
growth temperature and cold storage. HortScience 28, 1085–1086.
Pooler, M.R., Simon, P.W., 1994. True seed production in garlic. Sex. Plant Reprod. 7,
282–286.
Qu-Ying, H., Takagi, H., Ogasawara, N., Etoh, T., 1994. Development of types of inflo-
rescences of garlic and some Allium species. J. Jpn. Soc. Hortic. Sci. 63, 121–130
(in Japanese).
Rabinowitch, H.D., 1985. Onions and other edible Alliums. In: Halevy, A.H. (Ed.),
Handbook of Flowering, vol. 1. CRC Press, Boca Raton, Florida, pp. 398–409.
 D. Mathew et al. / Environmental and Experimental Botany 71 (2011) 166–173
Rabinowitch, H.D., 1990. Physiology of flowering. In: Rabinowitch, H.D., Brewster,
J.L. (Eds.), Onions and Allied Crops-I: Botany, Physiology and Genetics. CRC Press,
Boca Raton, Florida, pp. 398–409.
Rabinowitch, H.D., Kamenetsky, R., 2002. Shallot (Allium cepa, Aggregatum Group).
In: Rabinowitch, H.D., Currah, L. (Eds.), Allium Crop Science: Recent Advances.
CABI Publishing, Wallingford, Oxon, UK, pp. 409–430.
Rosen, C.J., Tong, C.B.S., 2001. Yield, dry matter partitioning, and storage quality of
hardneck garlic as affected by soil amendments and scape removal. HortScience
36, 1235–1239.
Shemesh, E., Scholten, O., Rabinowitch, H.D., Kamenetsky, R., 2008. Unlocking vari-
ability: inherent variation and developmental traits of garlic plants originated
from sexual reproduction. Planta 227, 1013–1024.
Simon, P.W., 2003. Realizing value from Central Asian Allium germplasm collections.
HortScience 38, 689.
Simon, P.W., Jenderek, M.M., 2003. Flowering, seed production, and the genesis of
garlic breeding. Plant Breeding Rev. 23, 211–243.
View publication stats
173
Takagi, H., 1990. Garlic Allium sativum L. In: Brewster, J.L., Rabinowitch, H.D. (Eds.),
Onions and Allied Crops, III, Biochemistry, Food Science, and Minor Crops. CRC
Press, Boca Raton, Florida, pp. 109–146.
Takagi, H., Qu-Ying, H., Etoh, T., 1993. Seed germination and seedling culture in fertile
garlic. Bull. Yamagata Univ. Agric. Sci. 11, 699–705.
Tukey, J.W., 1949. Comparing individual means in the analysis of variance. Biomet-
rics 5, 99–114.
Vieira, R.L., Nodari, R.O., 2007. Genetic Diversity of Garlic Revealed by RAPD Markers,
vol. 37. Ciência Rural, Santa Maria, pp. 51–57.
Volk, G.M., Henk, A.D., Richards, C.M., 2004. Genetic diversity among US garlic clones
as detected using AFLP methods. J. Am. Soc. Hortic. Sci. 129, 559–569.
Wang, C.-N., Cronk, Q.C.B., 2003. Meristem fate and bulbil formation in Titanotrichum
(Gesneriaceae). Am. J. Bot. 90, 1696–1707.