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Root Hair Growth and Development in Response to Nutrients and

Phytohormones

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Chapter 3
Root Hair Growth and Development
in Response to Nutrients
and Phytohormones

De-Jian Zhang, Yu-Jie Yang, Chun-Yan Liu, Fei Zhang,

and Qiang-Sheng Wu

3.1 Introduction

Root hairs are tip-growing extensions from root epidermal cell (Grierson and
Schiefelbein 2002). As extensions from root epidermis, root hairs can highly
increase root surface area and play important roles in nutrient and water absorption,
the interaction with soil microflora, such as arbuscular mycorrhizal (AM) fungi,
nitrogen-fixing bacteria, etc. (Grierson and Schiefelbein 2002; Libault et al. 2010;
Tanaka et al. 2014; Li et al. 2017; Vincent et al. 2017; Zou et al. 2017; Dolan 2017).
Especially, it is very important for the plant to absorb scarcely mobile soil minerals,
such as phosphorus (P) and potassium (K) from soil (Gahoonia et al. 1997; Gahoonia
and Nielsen 1998; Zuchi et al. 2011; Brown et al. 2012; Cao et al. 2013; Jungk
2015). Root hair has been demonstrated to be important for P acquisition in a number
of research papers in several crop species, particularly in low-P environment (Föhse
et al. 1991; Hoffmann and Jungk 1995; Bates and Lynch 1996; Gahoonia et al. 1997;
Bates and Lynch 2000; Yan et al. 2004; Brown et al. 2012). Furthermore, water
channels, as well as calcium, phosphate, potassium, etc., are localized in root hair,
and it has been suggested that root hair takes part in the absorption of most macro-
and micronutrients in a number of crop plants (Gilroy and Jones 2000; Libault et al.
2010). Even more, Wang et al. (2016) considered that long and dense root hairs are
important traits in ensuring efficient absorption of both macro- and micronutrients in
the early establishment of crops in nutrient-limited soil and low nutrient input
environment cropping systems.

De-Jian Zhang and Yu-Jie Yang contributed equally to this work.

D.-J. Zhang · Y.-J. Yang · C.-Y. Liu · F. Zhang · Qiang-ShengWu (*)

College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei, China
Institute of Root Biology, Yangtze University, Jingzhou, Hubei, China

© Springer International Publishing AG, part of Springer Nature 2018 65

B. Giri et al. (eds.), Root Biology, Soil Biology 52,
https://doi.org/10.1007/978-3-319-75910-4_3
66 D.-J. Zhang et al.

Fig. 3.1 Patterns of root hair development. (a) Cross section of a trichoblast (epidermal cell that
will produce a root hair) during root hair development. Note the nuclear movements accompanying
root hair emergence and changes in the organization of the cytoplasm at each new developmental
phase. (b) Divergence of root epidermal cell fate to trichoblast or atrichoblast might be determined
by asymmetrical division and differences in subsequent differentiation of the daughter cells or by
positional effects relative to underlying cell layers (Gilroy and Jones 2000)

3.2 Root Hair Development

Root hair development consists of four stages, viz., cell fate specification, initiation,
subsequent tip growth, and maturation (Gilroy and Jones 2000; Parker et al. 2000)
(Fig. 3.1).

3.2.1 Cell Fate Specification

The mechanism of epidermal cell fate to root hair has lucubrated in Arabidopsis
thaliana. Research evidence suggest genes, such as TRANSPARENT TESTA
GLABRA (TTG), WEREWOLF (WER) and GLABRA2 (GL2), are specific expression
in the non-hair epidermis cell and are negative transcriptional regulators of root hair
formation (Galway et al. 1994; Di et al. 1996; Masucci et al. 1996; Zhu et al. 2017).
Conversely the MYB-like transcription factor encoded by the CAPRICE (CPC) and
TRIPTYCHON (TRY) genes is thought to be specific expression in the non-hair
epidermis cell and is a positive regulator of root hair fate (Wada et al. 1997;
Schellmann et al. 2002; Schiefelbein 2003; Savage et al. 2008; Libault et al. 2010).
3 Root Hair Growth and Development in Response to Nutrients and Phytohormones 67

Fig. 3.2 The photos of cross and longitudinal section in the regions 2.0–3.0 cm from root apex of
the taproot of citrus. (A) E, epidermis cell; X, xylem; P, phloem; S, pith; (B, C) a, d, k, l, root hair
outgrow from epidermis cell which positioned over a single cortical cell; b, g, epidermis cell cannot
initiate root hair when located over two underlying cortical cells; c, h, epidermis cell cannot form
root hair when positioned over a single cortical cell; e, f, i, j, root hair form from epidermis cell
which is located over two underlying cortical cells (Zhang et al. 2013)

3.2.2 Root Hair Initiation

Root hair initiates from root epidermal cell. The initiation patterns of root hair have
been divided into three types (Clowes 2000; Kim et al. 2006a). In type 1, root hair
cell can differentiate from any epidermal cell (random type). The random type
pattern occurs throughout most dicots, many monocots, and most ferns’ plants,
such as Soleirolia soleirolii and Poncirus trifoliata (Fig. 3.2) (Clowes 2000;
Zhang et al. 2013). In type 2, the root epidermis consists of two sizes of cells,
long and short, but only the short cell differentiates into root hair cell (asymmetrical
cell division type). The asymmetrical cell division type occurs in monocots, basal
tracheophytes, and basal angiosperm families, such as Oryza sativa (Kim and Dolan
2011). Type 3 is position-dependent hair cell differentiation: root hair is located over
epidermal cell overlying the junction of two cortical cells, whereas non-hair cell is
located over a single cortical cell (positionally cued type) (Dolan et al. 1993; Galway
et al. 1994). This positionally cued type has been found in Brassicaceae and other
eudicot families, such as Arabidopsis (Cormack 1947; Clowes 2000; Dolan and
Costa 2001). In Arabidopsis, the epidermal cell overlying the junction of two cortical
cells was named as trichoblasts which could be initiated to root hair, while
atrichoblast was the epidermal cell located over a single cortical cell, which cannot
bulge to root hair (Duckett et al. 1994; Kwasniewski et al. 2013). Trichoblasts can be
distinguished from atrichoblasts by differences in their cytoplasmic structure in the
time of their formation in the meristematic zone, such as reduced vacuolation, etc.
(Galway et al. 1997).
68 D.-J. Zhang et al.

3.2.3 Root Hair Tip Growth

Following root hair initiation, it commences tip growth. During tip growth stage, the
deposition of new plasma membrane and cell wall material is confined to the
expanding tip, and the cytoplasm and pectic substance of the hair are highly
polarized, with secretory vesicles concentrated located behind the hair tip, followed
by the organelles required for the production and secretion of new cell wall and
plasma membrane materials (Galway et al. 1997; Carol and Dolan 2002, 2006). Ca2+
and cytoskeleton, annexins, calmodulin, GTPases, and protein kinases are the
candidate for the regulatory elements of the root hair tip-forced growth machinery
(Gilroy and Jones 2000). In the maturation stage, ribosomes, mitochondria, and
endoplasmic reticulum concentrate at the root hair tip (Cormack 1947; Nestler et al.
2014).

3.3 Root Hair Growth and Development in Response

to Nutrients

Recent studies have indicated that root hair growth and development could be
influenced by various environmental factors such as culture substrates (yellow soil,
Hoagland solution, etc.), mineral nutrients (nitrogen, phosphorus, potassium,
calcium, iron, magnesium, etc.), plant growth regulators (auxin, ethylene, jasmonic
acid, ethyl jasmonate, strigolactone, etc.), soil edaphon (arbuscular mycorrhizal
fungi, etc.), and so on (Zhu et al. 2006; Lee and Cho 2009; Libault et al. 2010;
Kapulnik et al. 2011; Niu et al. 2011; Yang et al. 2011; Peret et al. 2011; Muday et al.
2012; Wu and He 2011; Cao et al. 2013; Vandamme et al. 2013; Zhang et al. 2013;
Wu et al. 2016). Here, the effects of nutrients and phytohormones on root hair
growth and development have been detailed in the Introduction.

3.3.1 Nitrogen (N)

The NH4+ and NO3– are main N-compounds in soil for plants utilization (Forde
2002). With respect to NH4+ and NO3–, there is now clear molecular and electro-
physiological evidence that root hair could transport N-compounds. The expression
of two putative NH4+ and NO3– transporter genes (LeNRT1-2 and LeAMT1) is root
hair-specific in tomato, which is regulated by an external N supply1-38. In addition,
Meharg and Blatt (1995) have revealed that the high-affinity NO3– transporter in
Arabidopsis root hair is greatly upregulated under NO3– deficiency, indicating that
root hair provides adequate nutrients to the root. Direct evidence using SEM (scan-
ning electron microscope) has suggested that split root hair were initiated in
Arabidopsis thaliana after the addition of NH4NO3 to its roots (Yang et al. 2011).
3 Root Hair Growth and Development in Response to Nutrients and Phytohormones 69

Yang et al. (2011) consider that the effects of NH4+ and NO3– on split root hair may
through methyl jasmonate and ethylene signaling pathway that methyl jasmonate can
enhance the effect on split root hair while ethylene decrease it. Furthermore, NH4+
and NO3– may regulate calcium ion (Ca2+) in root hair cell through Rho-related
GTPase from plants (ROPs) and reactive oxygen species (ROS); however, Ca2+
gradient is indispensable for root hair tip growth (Shin et al. 2005; Bloch et al.
2011; Bai et al. 2014). Thus, N may have interactions with phytohormones, ROS,
or calcium ion in regulating root hair growth.

3.3.2 Phosphorus (P)

Phosphorus (P) is extremely immobile in soil and is frequently growth-limiting, and

it is an important macronutrient in plants, not only as a constituent of key cellular
molecules such as ATP, phospholipids, and nucleic acids but also playing a pivotal
role in energy conservation and metabolic regulation (Marschner 1995; Raghothama
and Karthikeyan 2005; Shin et al. 2005). Research efforts are now being focused on
understanding the mechanistic basis of P efficiency, to develop crops that require
less input.
Gahoonia et al. (1997) confirmed that root hairs can satisfy 60% of the plant’s P
demand in soil (Gahoonia and Nielsen 1998). P deficiency in the soil often induces
dense root hairs in plants such as Arabidopsis and citrus (Zhu et al. 2005; Cao et al.
2013). In P-deficient soil, the length and density of Arabidopsis root hairs increase
significantly, expanding the root’s surface area from 0.21 mm2 mm–1 root under
P-sufficient conditions to 1.44 mm2 mm–1 roots under P-starvation conditions, with
the root hairs constituting 91% of the total root’s surface area (Bates and Lynch
1996). In addition, the response to P deprivation in root hairs was accompanied by an
increase in ROS, which is necessary for root hair initiation and elongation through
Ca2+ gradient (Foreman et al. 2003; Shin et al. 2005; Carol and Dolan 2006). Thus,
there has interaction effect between ROS and P on root hair growth and
development.

3.3.3 Potassium (K)

Potassium ion (K+) is the most abundant cation in cells of higher plants, and it plays
a crucial role in plant growth and development, such as leaf movements, enzyme
homeostasis, photosynthesis, assimilate transport, enzyme activation, etc.
(Gassmann and Schroeder 1994; Miao et al. 2010). K deficiency not only reduces
crop resistance to pathogens, nutritional quality, and mechanical stability but also
decreases root hair growth, such as citrus root hair (Pettigrew 2008; Cao et al. 2013).
Gassmann and Schroeder (1994) considered that inward-rectifying K+ channels in
root hairs can function as both a physiologically important mechanism for
70 D.-J. Zhang et al.

low-affinity K+ uptake and as regulators of membrane potential. This evidence is a

major step toward a detailed molecular characterization of the multiple components
involved in K+ uptake, transport, and membrane potential control in root epidermal
cells.
TRH1 (AtKT/AtKUP/HAK K+ transporter family) was demonstrated in
Arabidopsis that its mutant trh1 has partially impaired in K+ transport, which also
blocked root hair growth and development (Rigas et al. 2001). However, the
defected root hair phenotype in trh1 could not restore when mutant seedlings were
grown at high external K concentrations (Rigas et al. 2001). It may demonstrate that
TRH1 mediates K+ transport in Arabidopsis roots and is responsible for specific K+
translocation, which is essential for root hair elongation (Rigas et al. 2001).
Interestingly, the researchers found that K interacts with phytohormones on root
hair growth and development, especially ethylene and auxin. When treated with K
starvation, both ethylene production and the transcription of genes involved in
ethylene biosynthesis were increased (Shin and Schachtman 2004; Jung et al.
2009). Ethylene signaling is a component of the plant’s response to low K that
stimulates the production of reactive oxygen species (ROS) and is important for
changes in root hair morphology and whole plant tolerance to low-potassium
conditions (Jung et al. 2009). With regard to auxin, Rigas et al. (2013) consider
that auxin modulates root hair morphogenesis at the differentiation zone. TRH1 (the
potassium transporter) was cell-specific subcellular localized in stele and epidermis,
which engagement in auxin transport and redistribution auxin (Rigas et al. 2013).
The role of the TRH1 in the sensing of external K+ and the regulation of potassium-
dependent root hair growth (Rigas et al. 2013). In Arabidopsis mutant trh1, auxin
imbalance caused poor root hairs (Vicente-Agullo et al. 2004; Rigas et al. 2013).
Hence, K may regulate root hair growth and development though the auxin
signaling.

3.3.4 Calcium (Ca)

Calcium ion (Ca2+) is involved in most biological processes in the plant kingdom
(Weinl and Kudla 2009). It serves as a second messenger and regulates a multitude
of adaptational, developmental, and physiological processes in plants, including cell
division, cell expansion, cytoplasmic streaming, responses to abiotic stress, adjust-
ment of ion homeostasis, and pathogen defense (Bush 1995; Sanders et al. 2002;
White and Broadley 2003; Kim et al. 2009). Cytoplasmic Ca2+ is known to regulate
cytoskeletal rearrangements and vesicular trafficking in tip-growing systems such as
root hair development system (Hepler et al. 2001). Early research has discovered that
the Ca2+ gradient existed in the growing root hairs, which is being most pronounced
in the rapidly elongating root hairs (Fig. 3.3) (Wymer et al. 1997). With regard to the
effect of Ca2+ on root hair growth, studies have shown that a growing root hair has a
localized gradient of Ca2+ concentration toward the growing apex, and the intensity
of this gradient correlates with the growth rate of the root hair (Schiefelbein et al.
3 Root Hair Growth and Development in Response to Nutrients and Phytohormones 71

Fig. 3.3 Gradients in cytoplasmic Ca2+ associated with tip growth of Arabidopsis root hairs
(Wymer et al. 1997). There are no detectable Ca2+ gradients in the stage of root hair initiation
(0 min) but on the stage of tip growth. The photos showed the Ca2+ gradients focused on the
elongating tip of root hair. Images are confocal ratio images of Arabidopsis root hairs loaded with
the fluorescent Ca2+ sensor Indo-1 and monitored using a confocal microscope. Ca2+ levels in the
cytoplasm have been color coded according to the inset scale. The arrow indicates the initiation
point of root hair. Scale bar ¼ 20 mm

1992; Pierson et al. 1996; Felle and Hepler 1997; Wymer et al. 1997; Takeda et al.
2008; Li et al. 2012). Electrophysiological studies, using the vibrating probe,
showed that Ca2+ influx was higher at root hair tip than at the base or sides of
growing root hair (Schiefelbein et al. 1992; Herrmann and Felle 1995; Jones et al.
1995). Based on confocal ratio imaging, Bibikova et al. (1997) demonstrated that a
tip-focused Ca2+ gradient was centered at the site of active growth. If the root hair
direction was changed, the Ca2+ gradient was also reoriented. Imposing an artificial
tip-focused Ca2+ gradient reorients root hair growth toward the new gradient
(Bibikova et al. 1997). These observations are all consistent with a model, whereby
a localized increase in Ca2+ at the root hair apex is specifically associated with
root hair growth (Gilroy and Jones 2000). Further evidence for the role of Ca2+,
using Ca2+ ionophores and channel blockers, suggested that disruption the Ca2+
concentration gradient result in inhibiting root hair tip growth (Miller et al. 1992;
Pierson et al. 1994; Herrmann and Felle 1995; Wymer et al. 1997).
With regard to the effect of ROS and Ca2+ on root hair growth and development,
Foreman et al. (2003) and Takeda et al. (2008) showed that ROS produced by
72 D.-J. Zhang et al.

NADPH oxidase activated Ca2+ channels in the apical plasma membrane, leading to
the tip-focused Ca2+ concentration gradient required for root hair polar growth.
Additional evidence from Arabidopsis rhd2 mutant indicated that application of
exogenous ROS to in vivo root apices stimulated cell growth and Ca2+ influxes in
root hair, which induced root hair elongation (Foreman et al. 2003). The positive
effect of exogenous ROS on root hair growth and development could be blocked by
pharmacological inhibitors of calcium channels (Foreman et al. 2003). Artificially
increasing cytosolic Ca2+ by treating with calcium ionophore A23187 (mixed
calcium-magnesium salt) induced production of elevated level of ROS around the
root hair tip and inhibited its tip growth for that these large amounts of ROS
disrupted the Ca2+ concentration gradient (Foreman et al. 2003).
As a consequence, Ca2+ concentration gradient is a requirement in sustaining root
hair tip growth, and ROS can activate calcium channel-mediated influx of Ca2+,
which creates a Ca2+ concentration gradient and subsequently influences root hair
elongation.

3.3.5 Iron (Fe)

Iron (Fe) is an essential nutrient for plants, which catalyzes crucial cellular functions
such as photosynthesis, chlorophyll synthesis, chloroplast development,
antioxidative cell protection, etc. (Siminis and Stavrakakis 2008; Curie and Mari
2017; Tsai and Schmidt 2017). Although Fe is one of the most abundant elements in
soils, it mainly exists as insoluble and nonavailable to plants (Tsai and Schmidt
2017). So plants have evolved efficient strategies to increase iron solubility and
absorption efficiency, such as increasing root hair (Muller and Schmidt 2004; Cao
et al. 2013). The number of root hairs was increased in response to Fe deficiency in
Arabidopsis and citrus (Muller and Schmidt 2004; Cao et al. 2013). Fe regulates root
hair growth and development through plant ferredoxin-like protein (PFLP), which
affects ROS content by NADPH oxidase (NOX) (Shin et al. 2011;
Sundaravelpandian et al. 2013; Nestler et al. 2014; Lin et al. 2015). Further evidence
suggests that Fe has interaction effect with ethylene on root hair initiation and
elongation. Fe deficiency can lead to the formation of extra root hairs located in
positions normally occupied by non-hair cells, which is dependent on ethylene
signaling and requires functional EIN2 and ETR1 genes (Schmidt and Schikora
2001).

3.3.6 Magnesium (Mg)

Magnesium (Mg) is an essential mineral nutrient for plant metabolic processes and
reactions, such as photophosphorylation, photooxidation in leaf tissues, chlorophyll
formation, protein synthesis, photosynthetic CO2 fixation, phloem loading, genera-
tion of ROS, and so forth (Cakmak and Yazici 2010). Mg is also involved in many
3 Root Hair Growth and Development in Response to Nutrients and Phytohormones 73

critical biochemical and physiological processes in plants, thus, influencing plant

growth and development (Cakmak and Yazici 2010; Gransee and Führs 2013).
Recently, the effect of interactions among Mg, ROS, and Ca2+ on root hair has
been reported. Low Mg availability resulted in longer and denser root hair in
Arabidopsis with greater concentrations of ROS and Ca2+ in the root tip and a
stronger Ca2+ concentration gradient in the root hair tip (Niu et al. 2014). However,
when treated with diphenylene iodonium (DPI, an NADPH oxidase inhibitor) or
1,2-bis(o-aminophenoxy) ethane-N,N,N0 ,N0 -tetraacetic acid (BAPTA, a Ca2+ chela-
tor), the Ca2+ concentration gradient was eliminated for the enhanced growth of root
hair in low-Mg treatment (Frahry and Schopfer 1998; Yoshioka et al. 2001; Kadota
et al. 2004). Instead, root hair growth was blocked in high-Mg treatment, and the
inhibiting effect was restored when supplied with CaCl2 or phenazine methosulfate
(PMS, a ROS generator) in Arabidopsis (Zhang et al. 2009; Niu et al. 2014). The
study outlined by Niu et al. (2014) showed that NADPH oxidase in root was
positively regulated by low Mg and was inhibited by high-Mg level, which further
evidenced that Mg could control ROS to regulate root hair growth and development.
Therefore, the growth and development of root hair is closely related to Mg
availability, which is through ROS and Ca2+ signaling.

3.4 Root Hair Growth and Development in Response

to Phytohormones

3.4.1 Auxins (IAAs)

The phytohormone auxins are a major determinant and regulatory component

important for plant growth and development (Kuhn et al. 2017). In particular,
auxin is considered the main signaling molecule involved in regulating root hair
growth (Pitts et al. 1998; Muday et al. 2012). Epidermal cell as cradle of root hair
needed adequate auxin for its initiation (Cho et al. 2007a; Lee and Cho 2009). In
Arabidopsis, the auxin response mutant axr1 has fewer and shorter root hairs, but
root hair growth can be dramatically promoted by exogenous auxins, such as
1-naphthylacetic acid (NAA) and indole-3-butyric acid (IBA) (Pitts et al. 1998;
Rahman et al. 2002; Muday et al. 2012). Auxin improved root hair density by
increased trichoblast number and the percentage of trichoblast bulged to root hair
(Masucci and Schiefelbein 1996; Niu et al. 2011; Lee and Cho 2013). Bruex et al.
(2012) found that 90% of genes related to root hair growth were positively regulated
by auxin based on transcriptome sequencing data analysis.
Auxin transport between cells is mediated by a complex system of transporters
such as AUXIN RESISTANT 1 (AUX1), LIKE AUX1 (LAX), Pin-formed (PIN), and
ATP-BINGING CASSETTE B (ABCB) genes, and their localization and activity are
thought to participate in root hair initiation and elongation (Rahman et al. 2002; Cho
et al. 2007a; Jones et al. 2009; Strader and Bartel 2009; Ganguly et al. 2010; Kuhn
et al. 2017). Auxin is primarily synthesized at the shoot apex, transferred toward the
74 D.-J. Zhang et al.

root tip by the vascular tissues of the stem, and moved basipetally to the elongation
zone through peripheral root tissues (Rigas et al. 2013). Such transportation can be
blocked by auxin transport inhibitors, such as 1-naphthoxyacetic acid (1-NOA),
2-naphthoxyacetic acid (2-NOA), and 3-chloro-4-hydroxyphenylacetic acid
(CHPAA) which regulate overall auxin transport (LaňKová et al. 2010). In addition,
auxin fluxes at the root apex are mainly controlled by various PIN auxin efflux
carriers, in addition to AUX1, LAX auxin influx carriers, and some members of the
ABCB transporters (auxin efflux genes) (Yang and Murphy 2009; Tromas and
Perrot-Rechenmann 2010; Swarup and Péret 2012). Auxin transport and auxin
synthesis are controlled by many genes, such as tryptophan aminotransferase related
(TAR) and flavin-containing monooxygenase (YUCs) (Mano and Nemoto 2012).
Understanding auxin biosynthesis and transport is an important factor in understand-
ing root hair growth. For instance, overexpression of YUCs in Arabidopsis enhanced
root hair growth, compared to the wild type (Zhao et al. 2001). In Arabidopsis
mutant ein2 (auxin efflux carrier), the auxin transportation channel from root tip to
root hair zone was blocked, which inhibited root hair initiation and elongation results
in short and thin root hairs (Cho et al. 2007b). In addition, Arabidopsis mutant aux1
also performs similar phenotype on root hair to ein2 (Strader et al. 2010).

3.4.2 Ethylene (ETH)

Ethylene is considered as the vital signal molecule involved in regulating develop-

ment and growth of root hair (Pitts et al. 1998; Muday et al. 2012). In Arabidopsis,
the ethylene response mutant ctr1 (the gene encodes a Raf-like protein kinase that
negatively regulates the ethylene signal transduction pathway) significantly reduced
the growth of root hairs (Kieber et al. 1993). Furthermore, 1-aminocyclopropane-1-
carboxylic acid (ACC, the ethylene precursor) increased root hair density and length,
whereas aminoethoxyvinylglycine (AVG, an ethylene biosynthesis inhibitor) and
AgNO3 (Ag, an ethylene action inhibitor) reduced root hair (Masucci and
Schiefelbein 1994; Tanimoto et al. 1995; Masucci and Schiefelbein 1996; Pitts
et al. 1998; Dolan 2001; Moeder et al. 2002; Zhu et al. 2006; Parimalan et al.
2011; Shah et al. 2014).
In Arabidopsis, ethylene effect improved the percentage of trichoblast to root hair
and promoted the initiation of ectopic root hair (Masucci and Schiefelbein 1996; Niu
et al. 2011; Lee and Cho 2013). EIN2 (Arabidopsis ethylene receptor resistant) is a
positive regulator of ethylene responses, which as an ethylene receptor participated
in inducing root hair formation (Lin et al. 2015; Zheng and Zhu 2016). Rahman et al.
(2002) have demonstrated that Arabidopsis mutant ein2 has short and thin root hairs.
ACS, an important role in the ethylene biosynthesis pathway, could catalyze the
conversion of AdoMet to ACC which is the precursor of ethylene (Moeder et al.
2002). Ribaudo et al. (2006) demonstrated that root hair grow through a mechanism
of ACS in tomato. Thus, ethylene-regulated root hair formation may be through its
biosynthesis, receptor, and signal transduction pathways.
3 Root Hair Growth and Development in Response to Nutrients and Phytohormones 75

However, the interaction between ethylene and auxin is more attractive for
scientist. Bruex et al. (2012) found that 90% of genes related to root hair growth
and development were upregulated by ethylene and auxin based on transcriptome
sequencing data analysis. In Arabidopsis, ACC increased root hair growth on auxin
response mutant axr1, while NAA could effectively relieve the inhibitory effect on
ethylene signal transduction mutant ein2 (Pitts et al. 1998; Rahman et al. 2002;
Muday et al. 2012). On the one hand, Michael (2001) proposed the hypothesis of
the “ethylene center in root hair development,” i.e., soil environment, growth regu-
lator, and mineral nutrients may control the effective endogenous ethylene concen-
tration in root hair cells and further regulate root hair growth. On the other hand,
endogenous auxin plays an important role in root hair growth, and its concentration
determines by its synthesis and transport efficiency, which are regulated by auxin
synthesis and transport genes (TAR2 and YUCs; AUX1, ABCBs, and LAXs) (Marchant
et al. 1999; Rahman et al. 2002; Cho et al. 2007a; Jones et al. 2009; Ganguly et al.
2010). Auxin could induce ethylene biosynthesis, which positively regulates root hair
growth (Yoshii and Imaseki 1982; Pitts et al. 1998; Muday et al. 2012). Ethylene also
could regulate auxin biosynthesis and transport-dependent auxin distribution that are
important for root and root hair initiation (Rahman et al. 2002; Cho et al. 2007a;
Růžička et al. 2007; Ganguly et al. 2010). Furthermore, ethylene promotes the
induction by auxin of the cortical microtubule randomization required for root hair
growth in Lactuca sativa (Takahashi et al. 2003). In citrus plant, Zhang et al. (2016)
confirmed that ethylene may positively regulate root hair growth by ethylene synthe-
sis, receptor, and signal transduction genes. Furthermore, it achieved a local activa-
tion of the auxin-signaling pathway and may regulate root hair growth by both
stimulating the auxin biosynthesis and modulating the auxin transport machinery
(Zhang et al. 2016). So, ethylene modulated root hair growth partially through auxin-
signaling pathway.

3.4.3 Jasmonic Acid and Methyl Jasmonate (JA and MeJA)

Besides auxin and ethylene, JAs and MeJAs also participate in root hair develop-
ment and growth. JA and MeJA could induce more bifurcate root hair, so they have a
pronounced effect on promoting root hair formation and elongation (Zhu et al.
2006). However, the effect of MeJA and JA on root hair formation and elongation
was dramatically diluted by ethylene inhibitors aminoethoxyvinylglycine (AVG)
and AgNO3 (Zhu et al. 2006). The enhancing effects of JA and MeJA were also
diminished in ethylene-insensitive mutant etr1. Furthermore, the JA biosynthesis
inhibitors ibuprofen and salicylhydroxamic acid (SHAM) not only decreased the
enhancing effect of ethylene precursor (1-aminocyclopropane-1-carboxylic acid,
ACC) on root hair initiation and elongation but also diminished the facilitating
effect on root hair growth in ethylene overproducing mutant eto1 (Zhu et al.
2006). So, there is an interaction between JA/MeJA and ethylene in the regulation
of root hair growth.
76 D.-J. Zhang et al.

Hentrich et al. (2013) demonstrated that JA-signaling pathway was linked to

auxin homeostasis through the regulation of the expression of auxin signal trans-
duction genes (YUCCA8 and YUCCA9). Because auxin is a major determinant and
regulatory component important for root hair growth and development (Kuhn et al.
2017). Thus, JAs and MeJAs may regulate root hair growth and development
through auxin-signaling pathway.

3.4.4 Strigolactone

Strigolactones (SLs) were originally isolated from plant root exudates as germina-
tion stimulants for root parasitic plants of the family Orobanchaceae, including
Alectra spp., Witchweeds (Striga spp.), and broomrapes (Orobanche and
Phelipanche spp.), and so were regarded as detrimental to the producing plants
(Gomezroldan et al. 2008; Xie et al. 2010; Waters et al. 2017). It has been recently
shown that SLs or their metabolites are a novel class of plant hormones that regulate
many aspects of shoot and root growth and development (Gomezroldan et al. 2008;
Xie et al. 2010; Waters et al. 2017). GR24, as a synthetic bioactive SL, could lead to
increased root hair length in Arabidopsis (Kapulnik et al. 2011). Additional studies
have suggested cross talk between SLs and auxin in determining root hair growth.
SLs might be involved in root hair tip growth via the modulation of auxin efflux in
roots by regulating in PINs and TIR1. Evidence in tomato roots suggested that SLs
interfered with the inhibitory effect of exogenously applied auxin on root hair
elongation and auxin efflux carriers were involved in this process (Koltai et al.
2010; Kapulnik et al. 2011; Mayzlish-Gati et al. 2012). However, excess GR24
could lead to disturbances in auxin efflux and hence to an excess in cellular
concentration of auxin; this, in turn, leads to reduction in the GR24 induction of
root hair elongation (Kapulnik et al. 2011). Thus, SLs have an additional hormonal
role in plants, acting as positive regulator of root hair growth and development.

3.4.5 Brassinosteroids

Brassinosteroids (BRs), compounds characterized as polyhydroxy steroids, are

natural substances that play vital roles in the regulation of metabolic processes
including respiration and in plant tolerance against abiotic stresses including water
deficit and cold stress (Derevyanchuk et al. 2015; Lima and Lobato 2017). Interest-
ingly, BRs have different effects on root hair growth and development, such as the
reduction of numbers and length of root hairs in Arabidopsis but positively regulat-
ing in Oryza sativa (Kim et al. 2006b; Hardtke et al. 2007). It has been demonstrated
that BR is required for cell proliferation in the root, and AXR3/IAA17 might be
involved in the BR-signaling pathway in root development (Mouchel et al. 2004,
2006; Kim et al. 2006b). In addition, the gain-of-function mutations of AXR3/IAA17
3 Root Hair Growth and Development in Response to Nutrients and Phytohormones 77

inhibited root hair growth and development (Knox et al. 2003). In brief, it suggests
that it has a cross talk of BR and auxin signaling in root hair growth and
development.

3.5 Future Perspectives and Conclusions

Improving plants to make root hair high efficiency of nutrients and water uptake
should reduce the environmental impact of agriculture as well as increase crop
production and quality. Even abundant research papers carry on deeper studying to
the effects of nutrients and phytohormones on root hair growth. But root hair
morphogenesis is driven by an amalgam of interacting processes controlled by
complex signaling events. Some of the major factors involved in the signaling
process during root hair growth and development have been identified, such as N, Ca
2+
, Mg2+, P, and so forth. It is not clear how these signaling component interactions
regulate root hair at the molecular and cellular level or how these signals interact
with phytohormones to regulate root hair growth and development, such as auxin,
ethylene, JAs, MeJAs, etc. Furthermore, the role of a Ca2+ gradient in root hair tip
growth is still scarce.
More works are needed to clone the genes of additional root hair mutants and
elucidate their roles, as well as add to our current knowledge of the signaling
networks involving nutrient and phytohormone regulation on root hair cell fate
specification, initiation, tip growth, and maturation by reverse genetics and mutant
complementation studies.

Acknowledgments This study was supported by the Yangtze Youth Fund (2016cqn64) and the
Yangtze Initial Fund (801190010132) of Yangtze University and the Plan in Scientific and
Technological Innovation Team of Outstanding Young, Hubei Provincial Department of Education
(T201604).

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