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Interactions of Phytohormones with Fiber Development: Comparison
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Please note this is a comparison between Version 2 by Jason Zhu and Version 1 by Masood Jan.
Phytohormones are small endogenous signal molecules in plants. Plant hormones are regulators of plant growth and development and are also particularly important in the establishment of fiber cells in cotton. Gibberellic acid (GA), jasmonic acid (JA), auxin, ethylene (ETH), and brassinosteroid (BR) all contribute to fiber formation, but cytokinin (CK) and abscisic acid (ABA) inhibit fiber growth. Studies of endogenous hormone levels have shown that plant hormones affect the formation of cotton fiber cells. Plant hormones have been shown to play important roles in the growth of cotton fiber cells and the retention of cotton bolls. Furthermore, measurements of hormone levels have shown that fiber cell initiation and elongation are linked. ESTs from ovules indicate that several phytohormone regulators contribute to the early stages of fiber growth, including auxin, BR, GA, and ABA. The expression of MIXTA, MYB5, GL2, and eight genes in the auxin, BR, GA, and ETH pathways is up-regulated when fiber cells begin to form, but the expression of these genes is down-regulated in the n1n1 mutant, which is not capable of making fibers. These findings are consistent with the well-known effects of phytohormones on fiber cell development in immature cotton ovules grown in vitro. Assembly of ESTs from fiber initials at 1 DPA has revealed several novel genes involved in fiber formation. In addition to CAPRICE (CPC) genes, many genes that regulate BRs, GTP-mediated signal transduction, cell cycle control, and components of a Ca2+-mediated signaling pathway have been identified in fiber at one DPA. This indicates that Ca2+ and other signaling pathways play a role in fiber development. It also suggests that the expression of phytohormonal pathway genes is activated before the expression of MYB-like genes is activated, which suggests that phytohormones play a key role in determining cell fate.
  • cotton (Gossypium spp.)
  • molecular mechanism
  • Phytohormones

1. Introduction

Cotton (Gossypium spp.) is a globally cultivated, economically important fiber crop. Cotton fibers are one of the main natural resources of the textile industry, and the quality of cotton fibers has a direct effect on the quality of cotton-based textiles [1]. Cotton is also a natural fiber and oil crop that can grow in diverse environments and provide a sustainable source of renewable resources. Upland cotton in particular is known for its high environmental adaptability and its ability to yield large quantities of fiber. Upland cotton has been widely planted, and its output accounts for approximately 95% of all planted cotton [2]. The elongation and development of cotton fibers are complex processes involving multiple genes and pathways. The environment has a substantial effect on the yield and quality of cotton fibers [3]. Because the quality of cotton fiber has a direct effect on the quality of textiles, improving the yield and quality of cotton fiber has long been a major goal of cotton domestication. Sequencing technology has become increasingly used in various scientific fields [4]. The development of mRNA sequencing technology, genome sequencing technology, resequencing technology, and phenotype evaluation methods for cotton has provided new tools for studying the biological mechanisms underlying cotton fiber elongation, and these new approaches could be used by cotton breeders to develop new varieties of upland cotton with improved fiber quality and yield, which would greatly benefit the global textile industry [5]. Transcriptomic analysis permits comparison of the levels of gene expression between cotton varieties at different developmental stages, and this information can be used to enhance fiber production [6,7][6][7]. Cotton fibers are single-celled protrusions from the epidermal layer of the ovules; the differentiation and development process can be divided into four overlapping periods: initiation, elongation, secondary cell wall (SCW) biogenesis, and dehydration maturity. The elongation of lint fibers begins at anthesis, whereas the elongation of fuzz fibers begins at 5–10 d post-anthesis (DPA); linear growth continues for approximately 20 d until a length of 25–30 mm is reached [8]. Elongation then ceases, and the secondary deposition of cellulose begins; however, significant overlap between these two processes is often observed [6]. Elongation of the second wave of fibers begins 5–10 d after anthesis, which results in fuzz fibers (referred to as “linters” in the cottonseed trade). These are usually relatively short and stick to the seed when they are ginned [7].
Recent studies of the morphology and embryology of cotton ovules have greatly enhanced ourthe understanding of cotton ovule development. Transmission electron microscopy has also been used to study the development of fibers [7,8][7][8]. The developmental morphology of cotton flowers and seeds has been examined using scanning electron microscopy. The formation of cotton ovules and fibers at anthesis has been examined in previous studies. However, not all elements of cotton ovule fiber formation have been discussed. Some previous studies provide detailed descriptions of the formation of early fibers and the surface of the cotton ovule at anthesis through scanning electron microscopy [7,9,10][7][9][10]. In Gossypium hirsutum, long lint fibers are produced before or on the day of anthesis (i.e., 0 DPA), although only 15–25% of epidermal cells form commercially usable textile lint fibers. Ovule epidermal cells that start at or after 3 DPA make shorter fibers called linters or fuzz that cannot be separated from seeds by ginning. Fiber mutants in which the growth or development of fiber initials is inhibited are useful tools in phenotypic surveys, as they have shown that the first detectable sign of fiber initiation occurs on the day of anthesis (i.e., 0 DPA). The ratio of fiber initials to total epidermal cells is approximately 25% [9], indicating that fiber output can be enhanced by increasing the number of initials. Breeders have learned that sucrose synthase (SUS) genes can be used to make cotton fibers that are of better quality [10,11][10][11]. The initiation mechanisms of lint and fuzz fibers involve genes such as MYB transcription factors (TFs) [11,12][11][12] and phytohormones such as auxin [13[13][14][15],14,15], gibberellic acid (GA) [11[11][16],16], brassinosteroid (BR) [17[17][18],18], ethylene (ETH) [3[3][15],15], abscisic acid (ABA) [10[10][13],13], and cytokinin (CK) [13,19][13][19]. Cotton fibers, which are used in the textile industry, have long been used to study cell elongation and cell wall biosynthesis [11]. Cotton is one of the world’s most important fiber crop plants and has long been studied. The sequencing of the cotton genome has provided a foundation for transcriptomic studies [11]. These studies have identified several genes (e.g., MYB25, SUS, HOX1, and HD1) that play a role in fiber initiation and growth [10]. This information could be used to enhance the quality and production of cotton fiber in various ways. Few papers have reviewed the genes involved in the initiation and growth of cotton fibers, as well as other cellular processes that affect fiber development [4].

2. Gibberellic Acid

GA is a key hormone involved in various biological processes in plants, including seed germination, root and stem growth, flower development, fruit ripening, and dormancy [45,46][20][21]. Exogenous GA administration enhances fiber elongation in cotton [47][22], and the application of a chemical that inhibits GA biosynthesis into ovulated culture results in few and short fibers [41][23]. The concentrations of indole-3-acetic acid (IAA) and ABA, which control fiber elongation during the fiber development stage, are both higher in naturally colored cotton under exogenous GA application. This affects fiber durability, micronaire, and maturation [29,48][24][25]. GA accumulation is also related to the elongation of cotton fibers. The number of GA molecules in fiber cells increases and decreases after flowering because GA functions in flower growth and fruit ripening [49][26]. Endogenous GA3 is significantly higher in long fiber cotton types than in medium and short fiber cotton varieties [50][27]. Overexpression of GA20-OXIDASE1 (GhGA20ox1), a key enzyme in GA biosynthesis, results in increased fiber production and the production of longer fibers in transgenic cotton by significantly increasing the content of GA3 and GA4 [50][27]. Studies of genes that respond to GA have been conducted to determine the function of GA in cell elongation [51][28]. Transgenic fiber cells overexpressing GA20 oxidase show much higher GhSUSA1 transcript levels than wild-type fiber cells. Furthermore, exogenous bioactive GA promotes GhSUSA1 transcription in fiber cells and hypocotyls [52][29]. These findings indicate that GA promotes the formation of SCW in cotton fiber cells by increasing the expression of sucrose synthase genes, which are required for cotton fiber elongation. A mechanism for how GA increases cotton fiber elongation has recently been described. When the GA level is low, one essential regulator in the GA signaling pathway, GhHOX3, interacts specifically with the GA suppressor GhSLR1 and prevents GhHOX3 from regulating target genes [12]. The interaction between GhHOX3 and GhHD1 then enhances the expression of two cell-wall-loosening genes. The HOX3 protein can increase the length of fibers by affecting GA signaling [49][26].

2. Jasmonic Acid

The jasmonic acid (JA) signaling pathway is involved in fiber initiation [53][30]. Cotton GhBLH7-D06 negatively regulates the resistance of cotton to Verticillium, and JA can induce the expression of GhBLH7-D06. Silencing GhBLH7-D06 can significantly increase the expression of genes involved in JA biosynthesis and signal transduction genes, such as GhLOX1-A08, GhLOX2-A05, and GhLOX3-A09, and enhance the resistance of cotton to Verticillium [44,54][31][32]. BLADE-ON-PETIOLE1 (BOP1) is a lateral organ boundary protein, and it can directly activate ATH1 under the action of cofactors to increase the content of JA in plants by promoting the expression of JA biosynthesis genes [39][33]. According to transcriptomic analysis, the overexpression of a GhJZA2 inhibitor in the JA signaling system results in reduced fiber initiation and shorter fibers [17], suggesting that the JA signaling pathway plays a key role in fiber elongation. Exogenous GA supplementation significantly increases fiber initiation and elongation. Furthermore, overexpression of GhJZA2 in G. hirsutum cv. YZ1 also decreases fiber initiation and results in shorter fibers [39][33].

3. Brassinosteroids

Brassinosteroids (BRs) are a class of polyhydroxylated steroidal phytohormones that play key roles in plant development, growth, and productivity [18]. These hormones regulate the division, elongation, and differentiation of numerous cell types throughout the entire plant life cycle [18,55][18][34]. BRs regulate the development of plants via TFs that either repress or induce the expression of downstream genes [11]. BRs play a critical role in the initiation and elongation of cotton fibers. The clearest evidence of the role of BR-induced gene expression in the production of cotton fiber comes from transgenic cotton plants overexpressing a cotton XTH called KC22. These plants generate fibers that are much longer than those produced by control plants. The synchronized addition of BRZ (a BR inhibitor) and BL (2,4-epibrassinolide) to cultured ovules partly restores fiber development, indicating that BRZ inactivates fiber development through its inhibitory effect on BR production [55][34]. In vitro treatment of BRs at low doses significantly increases fiber cell elongation; however, inhibiting the production of BRs leads to the inhibition of fiber cell growth [56][35]. The decrease in steroid levels caused by steroid 5-reductase (DET) is considered a crucial rate-limiting step in the production of BRs. GhDET2 suppression inhibits fiber cell initiation and elongation, and the seed-coat-specific expression of GhDET2 increases fiber length [39][33]. The exogenous administration of BL increases the elongation of cotton fibers. When flower buds are treated with BRZ, the rate of fiber cell morphogenesis decreases, which indicates that BRs play a role in fiber initiation and elongation. Furthermore, previous studies indicate that Gh14-3-3 proteins interact with GhBZR1 to modulate BR signaling, which controls fiber initiation and elongation [57][36]. bHLH/HLH TFs play a key role in fiber formation [58][37]. However, the specific mechanism by which bHLH/HLH TFs regulate BR signaling during fiber formation remains unclear. GhSK13 appears to be involved in the regulation of saccharide biosynthesis or metabolism, ETH signaling transduction pathway, actin/microtubule-related cytoskeleton, cell wall cytoskeleton status, as well as fatty acid synthesis/metabolism, which eventually affects cotton fiber development and quality. Fiber elongation is significantly suppressed by PDF1 [59,60][38][39]. The expression of these genes is down-regulated in pag1, which suggests that BR deficiency affects them. The inhibition of pag1 fiber elongation stems from the lower expression of GhPIP2 and PDF1. Furthermore, BRs directly or indirectly regulate fiber elongation-related factors such as VLCFA, ETH, the cytoskeleton, and cell-wall-related genes. Thus, BRs might determine the length of the fibers. Cotton fiber quality might be improved by manipulating BR homeostasis. Additional research is required to elucidate the biological activities of TFs in regulating BR signaling at various phases of cotton fiber initiation and elongation [18].

4. Auxins

Auxins are involved in various developmental processes in plants, including root growth, apical dominance, embryogenesis, vascular differentiation, and the response to internal and external stimuli [13,15][13][15]. Previous studies have shown that auxins accumulate in projecting cotton fiber cells, and overexpression of the auxin synthesis gene iaaM with an ovule-specific promoter increases the number of fiber initials, which results in a 15% increase in lint output and improved fiber fineness [3]. Auxin response factors (ARFs) are essential components in auxin signaling. ARFs bind to auxin response elements and control the expression of early auxin-responsive genes (AuxRE). At the beginning of the fiber formation process, the expression of ARFs from G. hirsutum in the GhARF2 and GhARF18 subfamilies, as well as six downstream TFs, is high [14,19][14][19]. In contrast to GhARF2 and GhARF18, GhIAA16, an IAA-induced protein, inhibits the formation of cotton fibers. The level of GhIAA16 expression is lower in mutant ovules than in wild-type ovules. However, the number of GhIAA16 transcripts is high in the fl mutant immediately after flowering [9]. Previous studies have shown that the expression of the auxin-binding protein GhABP is up-regulated (approximately 59-fold) in cotton between 0 and 10 DPA. GhABP expression has only been observed in elongated fibroblasts, and there is no evidence that GhABP is expressed in villous mutants or undifferentiated epidermal cells [61][40]. Although these findings suggest that GhABP plays a role in cotton fiber elongation, the biological function of ABP remains unknown. A comprehensive functional analysis is needed to clarify the biological function of the GhABP gene [62][41]. Several Rac genes have been identified in cotton. These genes are highly expressed in fibers and other elongated tissues during fiber elongation, unlike GhRac1, GhRac9, and GhRac13, and their expression decreases with the initiation of SCW biosynthesis [41,62][23][41]. The expression pattern of GhRac1 indicates that it might be involved in regulating the dynamics of the cytoskeleton in elongated fibers and other elongated tissues. GhRacA and GhRacB are widely expressed in the roots, stems, leaves, hypocotyls, and fiber cells, and the baseline expression of these two genes is highest in fiber cells as well as during elongation [63][42]. Furthermore, GhMPK6, a member of the MAPK family that plays a role in the responses of plants to many biotic and abiotic stresses, has been shown to affect fiber elongation through expression profile analysis. During fiber elongation, the phosphorylation level of GhMPK6 remains high, and phytohormones increase the phosphorylation level of GhMPK6 in the fibers [62,64][41][43].

6. Ethylene

Ethylene (ETH) plays various roles in plant growth and development, as well as in the responses of plants to biotic and abiotic stresses. ETH is known for its role in fruit ripening and organ abscission [11,44][11][31]. In cotton, ETH is thought to play a role in fiber cell initiation and growth, as shown by the overexpression of ACO genes during fiber elongation [65][44]. Furthermore, exogenous ETH stimulates fiber cell elongation. The expression of SUS, TUBULIN, and expansin genes is down-regulated in the Xu142 fl mutant, and down-regulation of the expression of these genes is required for cell wall formation, the cytoskeleton, and cell wall loosening [20][45]. ETH might promote cell elongation by modulating the expression of sucrose synthase, tubulin, and elongation-related proteins [29,66][24][46]. Although upland cotton (G. hirsutum) is the most common type of natural fiber, little is known about the regulation of fiber elongation. ETH production is a key biological process during fiber elongation according to the sequencing of a cotton fiber cDNA library and microarray analysis [29,67,68][24][47][48]. The expression of the key ETH-producing genes 1-aminocyclopropane-1-carboxylic acid oxidase1–3 (ACO1–3) is higher throughout this developmental phase compared with other developmental phases. The amount of ETH emitted by grown ovules is related to ACO expression and the rate of fiber development [20][45].

7. Cytokinin and Abscisic Acid

Levels of abscisic acid (ABA) and cytokinin (CK) are high in the ovules and developing fibers of a Ligon lintless (li) mutant line with short lint and normal fuzz, and this has been shown to inhibit fiber elongation and fiber initiation, respectively, in an in vitro ovule culture system [16[16][49],69], indicating that both hormones have antagonistic effects on cotton fiber development. ABA levels are also higher in the early stages of fiber formation in the Xu142 fl mutant [69][49]. Endogenous ABA levels in cotton ovules are positively linked to short fiber production. The deposition of ABA in 0 DPA ovules is significantly increased in the short fiber mutant Ligon lintless 2 (li2) compared with wild-type plants [70][50], indicating that ABA is a negative regulator of cotton fiber initiation and elongation. When the GhCKX gene is silenced with RNAi technology, the number of seeds increases significantly, and the fiber yield increases slightly, which indicates that CKs are needed for seed development and have an indirect effect on fiber yield [71][51].

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