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. 2011 Dec 1;6(12):1959–1962. doi: 10.4161/psb.6.12.18120

Progress on trichome development regulated by phytohormone signaling

Lijun An 1, Zhongjing Zhou 1, An Yan 1, Yinbo Gan 1,*
PMCID: PMC3337187  PMID: 22105030

Abstract

Trichomes are specialized structures that develop from epidermal cells in the aerial parts of plants, and are an excellent model system to study all aspects of cell differentiation including cell fate determination, cell cycle regulation, cell polarity and cell expansion. The development of the trichome is a process of integration of both external signals and endogenous developmental programs. During recent years, molecular analysis of trichome development at different stages has been well studied, and through the mutant phenotypes and the function of corresponding genes, the underlying mechanism has been revealed in a first glimpse. This paper offers a mini-view on this integration process with emphasis on the effects of plant hormone signaling on trichome development in plants through GLABROUS INFLORESCENCE STEMS (GIS) family and subfamily genes.

Keywords: cytokinin, GA, GIS, GL1, plant hormone, trichome development

In plants, the patterned assignment of alternative cell fates lies at the heart of many developmental processes. Understanding how neighboring cells in a developing tissue adopt distinct fates, therefore, presents a key challenge in plant development.1-3 The regulation of cell fate requires a balance of cell proliferation, differentiation, intercellular communication and morphogenesis control. Trichome development have provided a best model to explore the mechanisms that underlie the patterned assignment of cell fates during development in plants.1,2,4-6 Genetic and molecular analyses have been pursued in Arabidopsis thaliana to understand the regulation of cellular differentiation programs and have shown a network of transcriptional regulators that control the development of trichome in Arabidopsis.1,4-6

Regulation of Trichome Differentiation and Patterning via Phytohormones

In Arabidopsis, trichomes are large unicellular cells formed on the aerial parts of the plants including leaves, stems, branches and flower organs.7-9 They are likely to be differentiated from a field of initially equivalent cells, and finally regularly spaced and are rarely formed adjacent to one another, which suggest that some patterning mechanism regulations.2,4,10 Extensive experimental studies have uncovered a complex interlocked feedback network that operates within the epidermis to coordinate the choice between hair and nonhair fates.2-4,6,11,12 A ternary complex GLABRA1 (GL1)- GLABRA3(GL3)/ENHANCER OF GLABRA3 (EGL3)- TRANSPRENT TESTA GLABRA1 (TTG1) promotes the expression of GLABRA2 (GL2) to control the trichome development,4,13 meanwhile, the CAPRICE (CPC)-TRIPTYCHON (TRY)- ENHANCER OF TRY AND CPC 1 (ETC1)/ETC2 protein complex moves into neighboring cells where it inhibits trichome initiation by competing with GL1 for binding to GL3/EGL3, because neither the CPC-TRY-ETC1/ETC-GL3/EGL3-TTG1 complexes nor dissociated GL1 can promote GL2 or CPC-TRY-ETC1/ETC2 expression.2,4,6,11,12,14,15

The trichome differentiation is also regulated by phytohormones in plants, however, not much is known about the underlying mechanism of phytohormone signaling on the induction of trichomes.

Trichome initiation in Arabidopsis requires GA signaling and GA level response correlates positively with trichome number.16,17 The first evidence for the GA controlling trichome development comes from Chien and Sussex (1996) who demonstrated that application of GA to glabrous GA deficiency mutant gal-3 induces earlier trichome formation on the adaxial epidermis in compared with the abaxial epidermis. GL1 is the key transcriptional factor involving in controlling trichome initiation, and mutantion of GL1 results in the glabrous phenotype.18 SPINDLY (SPY) encodes a repressor of GA signaling,19,20 and the spy-5 mutant has more trichomes than the corresponding wild-type. The glabrous phenotype of gl1–1 spy-5 double mutant suggesting that GA signaling acts upstream of GL1 to trichome initiation,17 In consistent with this results, GL1 transcription is reduced in ga1–3 mutants, but can be significantly induced by the exogenous GA application.17 In addition, a C2H2 zinc finger protein coding transcription factor GLABAROUS INFLORESCENCE STEMS (GIS) also acts in a GA-responsive pathway to regulate trichome initiation in inflorescence organs.21 GIS act upstream of GL1 and downstream of SPY. In addition, GIS is antagonized in its action by the DELLA repressor GAI.21 Recently, a ZINC FINGER PROTEIN, ZFP5, was reported playing an important role in controlling trichome cell development also through GA signaling.22 The molecular analyses suggests that ZFP5 functions upstream of GIS, GIS2, (ZINC FINGER PROTEIN8) ZFP8, and also GL1 and GL3, and ZFP8 is characterized as the direct target of ZFP5 in controlling epidermal cell differentiation.

Cytokinins also increase trichome formation especially on inflorescence stems, and the influence of cytokinins increase as the inflorescence grows, and this effect is counteracted by mutations in SPY, which positively regulates cytokinin signaling.4,23 The control of cytokinins on trichome production requires two genes expressed in late inflorescence organs, ZFP8 and GIS2, which encode C2H2 transcription factors related to GIS.24 Cytokinin inducible GIS2 act downstream of SPY and upstream of GL1. GIS2 and ZFP8 also interacted with GIS to integrated GA and cytokinin singals in the regulation of trichome cell fate by collectively regulating GL1 expression.24 The proteins of GIS, GIS2 and ZFP8 are largely equivalent in function, but the genes have specialized and are differentially regulated during inflorescence development.24

Jasmonic acid and salicylic acid function as key signaling molecules in the induction of resistance to herbivoures and pathogenssignal transduction pathways, and are also involved in trichome formation in Arabidopsis.25-28 JA has a positive effect on the trichome density and number of newly produced leaves. Moreover, the adenylated jasmonic acid is not necessary for constitutive trichome production or the induction of tirchome, because the jar-1 mutant, which is unable to adenylate jasmonic acid,29 exhibited normal trichome induction following treatment with JA.28 JAZ proteins interact with GL3,EGL3, R2R3 MYB transcription factors MYB75 and GL1 to repress JA-regulated anthocyanin accumulation and trichome initiation.30

Salicylic acid or a downstream component reduced trichome density and number on new leaves based on the observation of the exogenously applied salicylic acid experiment.28 In consistent, the cpr mutant of Arabidopsis, which overexpresses salicylic acid, has reduced trichome densities.28,31 In addition to directly inhibiting trichome production, salicylic acid reduced the positive effects of jasmonic acid on trichome induction,28 suggesting negative cross-talk between the jasmonate and salicylate-dependent pathways.

There are is also evidence for interactions among gibberellin, jasmonic acid and salicylic acid pathways. GA and jasmonic acid are synergistic associated in the induction of trichomes, but salicylic acid is antagonized the induction of gibberellin in trichome density and number.28

Regulation of Trichome Growth via Phytohormones

After cell fate determination, the trichome progenitor cell stops the mitotic cycle and switch to endoreduplication, and then for branching and expansion. A mature trichome of Arabidopsis in leaves will proceed through four endoreduplication cycles and reached a DNA content of 32C (C equals haploid DNA content per nucleus), and with three branches.8,11,32,33 The underlying molecular mechanism in this process has been extensively studied and several mutants have been characterized in affecting the change from mitosis to endoredupication, the number of endoreduplication cycles, trichome branching and trichome expansion.4,6,11 SIAMASE (SIM) and STICHEL (STI) are two key regulators contribute to endoreduplication and trichome branching, respectively.34-37 SIM, a repressor of mitosis in the endoreduplication cell cycle,35 can cooperate with D-type cyclin (CYC)-CDKA;1 complex and CCS52/Fizzy-Related (FZR) family protein to establish endoreduplication in trichomes.38-43 STI regulates trichome branch number in an endoreduplication-independent pathway.36,44 TRY acts upstream of STI to restrict branching and has also been proposed to negatively affect GL3,45 which is also involved in endoreduplication.8,44,46

Trichome branching are known to be positively modulated by the endogenous GA levels and activity of its signal transduction pathways.17 Most of the trichomes in ga1–3 mutant background are two-branched in leaves. In contrast, application of exogenous GA to ga1–3 plants can restore its mutation phenotypes.16,17 In contrast, spy-5 mutant makes significantly over-branched trichomes on leaves.16,17 DNA content analysis of isolated trichomes indicate that spy-5 over branched trichomes indeed have twice as much DNA as wild-type trichomes on average, while ga1–3, like gl1–1 and ttg-1, exhibits 2C to 16C ploidy levels.17 The high frequency of over-branched trichomes on spy-5 leaves could be explained by an over activation of the endogenous GA-regulated GL1 gene which in turn could induce extra rounds of endoreduplication leading to extra branch formation.17 However, the regulation of GL1 by GA in regulating trichome branching in a direct or indirect way is still unknown. In addition, GA also plays role in regulation fiber elongation, which is trichome of cotton ovules, in cotton, because in vitro application of GA promotes fiber elongation.47

Ethylene also affect trichome branching, because an Arabidopsis loss-of-function ethylene receptor mutant, etr2–3, which has completely unbranched trichomes.44 It was hypothesized that ETR2 might affect the assembly of the microtubule cytoskeleton, and is positioned upstream of CHROMATIN ASSEMBLY FACTOR1 (CAF1) and TRY and is independent of the GL2 and GL3 pathways.44

Conclusions and Further Prospects

It has become evident that trichome patterning and the later growth process cannot be explained by one simple model. It seems to be governed by several principles in parallel, especially the response and interaction of the epidermis to plant hormones (Fig. 1). Future research will be essential to address several unclear issues in the regulatory network in trichome development and a further interplay between experimental and theoretical biologists will be necessary to elucidate these questions:

Figure 1.

Figure 1.

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Summary of phytohormone pathways in regulation trichome development. The arrow headed lines indicate the upregulation, and the blunted lines indicate the downregulation or inhibition.

1. Almost every kind of plant hormone discovered has functions in regulating trichome patterning and growth, but to our knowledge; there is no report about auxin and ABA in regulating trichome development. Do these hormones have a function in trichome development, and if so, what is the underlying mechanism?

2. The complex regulation of the endoreduplication cycle in trichomes by several different molecular pathways remains an important unknown.

3. The precise downstream target of the plant hormones in regulating trichome development still needs to be characterized.

Acknowledgments

We are in debt to Prof. Martin Hülskamp from University of Cologne, Germany and Dr. Clare Steele-King from University of York, for critical reading of the manuscript. The research was supported by National Natural Science Foundation of China (Grant No. 30970167; 31000093); Transgenic Plant Breeding Program of China (2009ZX08005-01B); Zhejiang Provincial Natural Science Foundation of China (Grant No. Z31100041) ; and Ph.D. Programs Foundation of Ministry of Education of China (Grant No. 20090101110097).

Glossary

Abbreviations:

DNA

Deoxyribonucleic acid

Footnotes

Reference

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