Advances in Regulatory Mechanism of Brassinolide on Plant Root Development

doi:10.13304/j.nykjdb.2020.0836

Abstract

Abstract:

Brassinosteroids （BRs） are new plant hormones discovered in the late 20 century. They are involved in regulating many aspects of plant growth and development， and have important regulatory roles in plant root development. Brassinolide （BL） is the first highly active BR which structure has been determined. This review first introduced the discovery of BR， the study of the signal pathway of BR on regulating root growth， and further elaborated the research progress of BR pathway transcription factors interacting with auxin， cytokinin （CTK）， ethylene （ETH） and other signaling molecules to regulate root stem cell niche， root apical meristem， root cell elongation， lateral roots， root hairs， and root gravitropic. And it also put forward questions and prospects for the in-depth study of BR's regulation in plant root development. The review provided a theoretical basis for the application of BR in regulating plant root development.

Key words: brassinosteroid, plant hormones, transcription factors, root development, action mechanism

摘要：

油菜素甾醇（brassinosteroids，BRs）是20世纪后期发现的一类新型植物激素，参与调控植物生长发育的诸多方面，其中对植物根系发育过程具有重要的调控作用。油菜素内酯（brassinolide，BL）是最先确定结构的高活性BR。首先介绍了BR的发现、BR调控根系生长信号通路的进展，进一步阐述了BR通路转录因子与生长素（auxin）、细胞分裂素（cytokinin，CTK）、乙烯（ethylene，ETH）及其他信号分子互作对调控根系干细胞生态位、根尖分生区、根细胞生长、侧根、根毛以及根系向地性的作用机制，并对BR调控植物根系发育的深入研究提出问题及展望，为BR在调控植物根系发育中的应用提供理论依据。

关键词: 油菜素内酯, 植物激素, 转录因子, 根系发育, 作用机理

CLC Number:

S636

Zhiyong WU, Hong GU, Dawei CHENG, Lan LI, Shasha HE, Ming LI, Jinyong CHEN. Advances in Regulatory Mechanism of Brassinolide on Plant Root Development[J]. Journal of Agricultural Science and Technology, 2022, 24(2): 68-76.

吴志勇, 顾红, 程大伟, 李兰, 何莎莎, 李明, 陈锦永. 油菜素内酯调控植物根系发育机制研究进展[J]. 中国农业科技导报, 2022, 24(2): 68-76.

Figures/Tables 5

Fig.1 BR regulates root stem cell niche［21］

Fig.2 BR regulates root apical meristem

Fig.3 BR regulates root cell elongation

Fig.4 BR regulates lateral root growth and development

Fig.5 BR regulates root hair growth and development［33］

References 74

1	SOPHIE D D， BRIAN F， LOÏC P， et al.. Root system architecture： opportunities and constraints for genetic improvement of crops ［J］. Trends Plant Sci.， 2007， 12（10）：474-481.
2	STEPHEN D， CHRISTIAN S H. Hormone signalling crosstalk in plant growth regulation ［J］. Curr. Biol.， 2011， 21（9）：R365-R373.
3	MITCHELL J W， MANDAVA N， WORLEY J F， et al.. Brassins—a new family of plant hormones from rape pollen ［J］. Nature， 1970， 225（5237）：1065-1066.
4	GROVE M D， SPENCER G F， ROHWEDDER W K， et al.. Brassinolide， a plant growth-promoting steroid isolated from Brassicanapus pollen ［J］. Nature， 1979， 281（5728）：216-217.
5	ANDRZEJ B， ANDRZEJ T. The chemical characteristic and distribution of brassinosteroids in plants ［J］. Phytochemistry， 2003， 62（7）：1027-1046.
6	WANG X F， GOSHE M B， SODERBLOM E J， et al.. Identification and functional analysis of in vivo phosphorylation sites of the Arabidopsis BRASSINOSTEROID-INSENSITIVE 1 receptor kinase ［J］. Plant Cell， 2005， 17（6）：1685-1703.
7	KYOUNG H N， LI J M. BRI1/BAK1， a receptor kinase pair mediating brassinosteroid signaling ［J］. Cell， 2002， 110（2）：203-212.
8	WHIPPO C W， HANGARTER R P. A brassinosteroid-hypersensitive mutant of BAK1 indicates that a convergence of photomorphogenic and hormonal signaling modulates phototropism ［J］. Plant Physiol.， 2005， 139（1）：448-457.
9	KARLOVA R， DE V S C. Advances in understanding brassinosteroid signaling ［J/OL］. Sci. STKE， 2006（354）：pe36 ［2021-07-05］. .
10	WANG X L， LI X Q， MEISENHELDER J， et al.. Autoregulation and homodimerization are involved in the activation of the plant steroid receptor BRI1 ［J］. Dev. Cell， 2005， 8（6）：855-865.
11	YIN Y H， WANG Z Y， SANTIAGO M G， et al.. BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation ［J］. Cell， 2002， 109（2）：181-191.
12	HE J X， JOSHUA M. G， YU S， et al.. BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses ［J］. Science， 2005， 307（5715）：1634-1638.
13	LI J， WEN J Q， LEASE K A， et al.. BAK1， an Arabidopsis LRR receptor-like protein kinase， interacts with BRI1 and modulates brassinosteroid signaling ［J］. Cell， 2002， 110（2）：213-222.
14	YU X F， LI L， LI L， et al.. Modulation of brassinosteroid-regulated gene expression by jumonji domain-containing proteins ELF6 and REF6 in Arabidopsis ［J］. Proc. Natl. Acad. Sci. USA， 2008， 105（21）：7618-7623.
15	LI J， NAM K H， VAFEADOS D， et al.. BIN2， a new brassinosteroid-insensitive locus in Arabidopsis ［J］. Plant Physiol.， 2001， 127（1）：14-22.
16	LI J， NAM K H. Regulation of brassinosteroid signaling by a GSK3/SHAGGY-Like kinase ［J］. Science， 2002， 295（5558）：1299-1301.
17	YIN Y H， VAFEADOS D， TAO Y， et al.. A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis ［J］. Cell， 2005， 120（2）：249-259.
18	GAMPALA S S， KIM T W， HE J X， et al.. An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis ［J］. Dev. Cell， 2007， 13（2）：177-189.
19	PENG P， YAN Z Y， ZHU Y Y， et al.. Regulation of the Arabidopsis GSK3-like kinase BRASSINOSTEROID-INSENSITIVE 2 through proteasome-mediated protein degradation ［J］. Mol. Plant， 2008， 1（2）：338-346.
20	MORA G S， VERT G， YIN Y H， et al.. Nuclear protein phosphatases with kelch-repeat domains modulate the response to brassinosteroids in Arabidopsis ［J］. Genes Dev.， 2004， 18（4）：338-346.
21	LOZANO E F， PLANAS R A， VILARRASA B J， et al.. Paracrine brassinosteroid signaling at the stem cell niche controls cellular regeneration ［J/OL］. J. Cell Sci.， 2018， 131（2）： jcs204065 ［2021-07-05］. .
22	GONZÁLEZ G M P， VILARRASA B J， ZHIPONOVA M， et al.. Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots ［J］. Development， 2011， 138（5）：49-859.
23	NORMA F， NA L， SJEF B， et al.. The BRASSINOSTEROID INSENSITIVE1-LIKE3 signalosome complex regulates Arabidopsis root development ［J］. Plant Cell， 2013， 25（9）：3377-3388.
24	VILARRASA B J， GONZÁLEZ G M P， FRIGOLA D， et al.. Regulation of plant stem cell quiescence by a brassinosteroid signaling module ［J］. Dev. Cell， 2014， 30（1）：36-47.
25	ESPINOSA R A， MARTíNEZ C， DE L M， et al.. Topless mediates brassinosteroid control of shoot boundaries and root meristem development in Arabidopsisthaliana ［J］. Development， 2017， 144（9）：1619-1628.
26	LEE H S， KIM Y， PHAM G， et al.. Brassinazole resistant 1 （BZR1）-dependent brassinosteroid signalling pathway leads to ectopic activation of quiescent cell division and suppresses columella stem cell differentiation ［J］. J. Exp. Bot.， 2015， 66（15）：4835-4849.
27	JEFRI H， TOON C， FILIP V， et al.. ERF115 controls root quiescent center cell division and stem cell replenishment ［J］. Science， 2013， 342（6160）：860-863.
28	MITSUHIRO A， DIMITRIS B， RENZE H， et al.. The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche ［J］. Cell， 2004， 119（1）：109-120.
29	CARLA G， HUGO H， MARIJN L， et al.. Plethora proteins as dose-dependent master regulators of Arabidopsis root development ［J］. Nature， 2007， 449（7165）：1053-1057.
30	JUTHAMAS C， WANG Z Y. Spatiotemporal brassinosteroid signaling and antagonism with auxin pattern stem cell dynamics in Arabidopsis roots ［J］. Curr. Biol.， 2015， 25（8）：1031-1042.
31	TIAN Y C， FAN M， QIN Z X， et al.. Hydrogen peroxide positively regulates brassinosteroid signaling through oxidation of the BRASSINAZOLE-RESISTANT1 transcription factor ［J/OL］. Nat. Commun.， 2018， 9（1）：1063［2021-07-05］. .
32	LYU B S， TIAN H Y， ZHANG F， et al.. Brassinosteroids regulate root growth by controlling reactive oxygen species homeostasis and dual effect on ethylene synthesis in Arabidopsis ［J/OL］. PLOS Genet.， 2018， 14（1）：e1007144 ［2021-07-05］. .
33	ACKERMAN-LAVERT M, FRIDMAN Y, MATOSEVICH R, et al.. Auxin requirements for a meristematic state in roots depend on a dual brassinosteroid function [J]. Curr. Biol., 2021, 31(20): 4462-4472.
34	HACHAM Y， HOLLAND N， BUTTERFIELD C， et al.. Brassinosteroid perception in the epidermis controls root meristem size ［J］. Development， 2011， 138（5）：839-848.
35	VRAGOVIĆ K， SELA A， FRIEDLANDER S L， et al.. Translatome analyses capture of opposing tissue-specific brassinosteroid signals orchestrating root meristem differentiation ［J］. Proc. Natl. Acad. Sci. USA， 2015， 112（3）：923-928.
36	RAFFAELE D I， FRANCISCO S L， EMANUELE S， et al.. Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation ［J］. Curr. Biol.， 2007， 17（8）：678-682.
37	MOUBAYIDIN L， PERILLI S， DELLO I R， et al.. The rate of cell differentiation controls the Arabidopsis root meristem growth phase ［J］. Curr. Biol.， 2010， 20（12）：1138-1143.
38	CÉLINE F M， KAREN S O， CHRISTIAN S H. BRX mediates feedback between brassinosteroid levels and auxin signalling in root growth ［J］. Nature， 2006， 443（7110）：458-461.
39	SCACCHI E， SALINAS P， GUJAS B， et al.. Spatio-temporal sequence of cross-regulatory events in root meristem growth ［J］. Proc. Natl. Acad. Sci. USA， 2010， 107（52）：22734-22739.
40	RAFFAELE D I， KINU N， LAILA M， et al.. A genetic framework for the control of cell division and differentiation in the root meristem ［J］. Science ， 2008， 322（5906）：1380-1384.
41	LI T T， KANG X K， LEI W， et al.. SHY2 as a node in the regulation of root meristem development by auxin， brassinosteroids， and cytokinin ［J］. J. Integr. Plant Biol.， 2020， 62（10）：1500-1517.
42	FRIDMAN Y， ELKOUBY L， HOLLAND N， et al.. Root growth is modulated by differential hormonal sensitivity in neighboring cells ［J］. Genes Dev.， 2014， 28（8）：912-920.
43	TÁBATA B， MARCIO C S， DANIEL S M. Antagonistic relationship between AtRALF1 and brassinosteroid regulates cellexpansion-related genes ［J/OL］. Plant Signal. Behav.， 2014， 9（10）：e976146 ［2021-07-05］. .
44	JIA Z T， GISHL R F H， MEYER R C， et al.. Natural variation of BSK3 tunes brassinosteroid signaling to regulate root foraging under low nitrogen ［J］. Nat. Commun.， 2019， 10（1）：2378 ［2021-07-05］. .
45	BAO F， SHEN J J， BRADY S R， et al.. Brassinosteroids interact with auxin to promote lateral root development in Arabidopsis ［J］. Plant Physiol.， 2004， 134（4）：1624-1631.
46	GUPTA A， SINGH M， LAXMI A. Interaction between glucose and brassinosteroid during the regulation of lateral root development in Arabidopsis ［J］. Plant Physiol.， 2015， 168（1）：307-320.
47	PUNA M M， BURKHARD S， SUNGHWA C. BIN2/DWF12 antagonistically transduces brassinosteroid and auxin signals in the roots of Arabidopsis ［J］. J. Plant Biol.， 2011， 54（2）：126-134.
48	YUYA Y， KIWAMU T， WATARU F， et al.. Transcription of DWARF4 plays a crucial role in auxin-regulated root elongation in addition to brassinosteroid homeostasis in Arabidopsis thaliana ［J/OL］. PLoS One， 2011， 6（8）：e23851 ［2021-07-05］. .
49	HYUNWÒO C， HOJIN R， SANGCHUL R， et al.. A secreted peptide acts on BIN2-mediated phosphorylation of ARFs to potentiate auxin response during lateral root development ［J］. Nat. Cell Biol.， 2014， 16（1）：66-76.
50	KIM M H， KIM Y， KIM J W， et al.. Identification of Arabidopsis BAK1-associating receptor-like kinase 1 （BARK1） and characterization of its gene expression and brassinosteroid-regulated root phenotypes ［J］. Plant Cell Physiol.， 2013， 54（10）：1620-1634.
51	TÁBATA B， BIANCA R， PAULO H O C， et al.. Moura. Arabidopsis thaliana RALF1 opposes brassinosteroid effects on root cell elongation and lateral root formation ［J］. J. Exp. Bot.， 2014， 65（8）：2219-2230.
52	HU Y X， WANG Y H， LIU X F， et al.. Arabidopsis RAV1 is down-regulated by brassinosteroid and may act as a negative regulator during plant development ［J］. Cell Res.， 2004， 14（1）：8-15.
53	JEONG S Y， PARK C H， KIM M K， et al.. Effect of Lysophosphatidylethanolamine and brassinosteroids on development of Arabidopsis roots ［J］. J. Plant Biol.， 2012， 55（2）：178-184.
54	VERCRUYSSEN L， GONZALEZ N， WERNER T， et al.. Combining enhanced root and shoot growth reveals cross talk between pathways that control plant organ size in Arabidopsis ［J］. Plant Physiol.， 2011， 155（3）：1339-1352.
55	CHANG L， RAMIREDDY E， SCHMÜLLING T. Lateral root formation and growth of Arabidopsis is redundantly regulated by cytokinin metabolism and signalling genes ［J］. J. Exp. Bot.， 2013， 64（16）：5021-5032.
56	DENG Q， WANG X， ZHANG D Z， et al.. BRS1 function in facilitating lateral Root emergence in Arabidopsis ［J/OL］. Int. J. Mol. Sci.， 2017， 18（7）：1549.［2021-07-05］. .
57	GALWAY M E， MASUCCI J D， LLOYD A M， et al.. The TTG gene is required to specify epidermal cell fate and cell patterning in the Arabidopsis root ［J］. Dev. Biol.， 1994， 166（2）：740-754.
58	DOLAN L， DUCKETT C M， GRIERSON C S， et al.. Clonal relationships and cell patterning in the root epidermis of Arabidopsis ［J］. Development， 1994， 120（9）：2465-2474.
59	ISHIDA T， KURATA T， OKADA K， et al.. A genetic regulatory network in the development of trichomes and root hairs ［J］. Annu. Rev. Plant Biol.， 2008， 59（1）：365-386.
60	RERIE W G， FELDMANN K A， MARKS M D. The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis ［J］. Genes Dev.， 1994， 8（12）：1388-1399.
61	WALKER A R， DAVISON P A， BOLOGNESI W A C， et al.. The TRANSPARENT TESTA GLABRA1locus， which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis， encodes a WD40 repeat protein ［J］. Plant Cell， 1999， 11（7）：1337-1349.
62	LEE M M， SCHIEFELBEIN J. WEREWOLF， a MYB-related protein in Arabidopsis， is a position-dependent regulator of epidermal cell patterning ［J］. Cell， 1999， 99（5）：473-483.
63	BERNHARDT C， LEE M M， GONZALEZ A， et al.. The bHLH genes GLABRA3 （GL3） and ENHANCER OF GLABRA3 （EGL3） specify epidermal cell fate in the Arabidopsis root ［J］. Development， 2003， 130（26）：6431-6439.
64	KIRIKI V， SIMON M， HUELSKAMP M， et al.. The ENHANCER OF TRY AND CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis ［J］. Dev. Biol.， 2004， 268（2）：506-513.
65	KUPPUSAMY K T， CHEN A Y， NEMHAUSER J L. Steroids are required for epidermal cell fate establishment in Arabidopsis roots ［J］. Proc. Natl. Acad. Sci. USA， 2009， 106（19）：8073-8076.
66	CHENG Y W， ZHU W J， CHEN Y X， et al.. Brassinosteroids control root epidermal cell fate via direct regulation of a MYB-bHLH-WD40 complex by GSK3-like kinases ［J/OL］. Elife， 2014， 25（3）：e02525［2021-07-05］. .
67	BORASSI C， DOROSZ J G， RICARDI M M， et al.. A cell surface arabinogalactan-peptide influences root hair cell fate ［J］. New Phytol.， 2020， 227（3）：732-743.
68	LI L， XU J， XU Z H， et al.. Brassinosteroids stimulate plant tropisms through modulation of polar auxin transport in Brassica and Arabidopsis ［J］. Plant Cell， 2005， 17（10）：2738-2753.
69	KIM T W， LEE S M， JOO S H， et al.. Elongation and gravitropic responses of Arabidopsis roots are regulated by brassinolide and IAA ［J］. Plant Cell Environ.， 2007， 30（6）：679-689.
70	LANZA M， GARCIA-PONCE B， CASTRILLO， et al.. Role of actin cytoskeleton in brassinosteroid signaling and in its integration with the auxin response in plants ［J］. Dev. Cell， 2012， 22（6）：1275-1285.
71	RETZER K， AKHMANOVA M， KONSTANTINOVA N， et al.. Brassinosteroid signaling delimits root gravitropism via sorting of the Arabidopsis PIN2 auxin transporter ［J］. Nat. Commun.， 2019， 10（1）：5516 ［2021-07-05］. .
72	SINGH M， GUPTA A， LAXMI A. Glucose control of root growth direction in Arabidopsis thaliana ［J］. J. Exp. Bot.， 2014， 65（12）：2981-2993.
73	SINGH M， GUPTA A， LAXMI A. Glucose and phytohormone interplay in controlling root directional growth in Arabidopsis ［J/OL］. Plant Signal. Behav.， 2014， 9（7）：e29219 ［2021-07-05］. .
74	XUE S， ZOU J J， LIU Y F， et al.. Involvement of BIG5 and BIG3 in BRI1 trafficking reveals diverse functions of BIG-subfamily ARF-GEFs in plant growth and gravitropism ［J/OL］. Int. J. Mol. Sci.， 2019， 20（9）：2339 ［2021-07-05］. .

[1]	DING Danyang, ZHANG Yijie, WANG Kaiyue, LIU Zhihong, LU Yutong, SHAO Huifang*. Physiological Achine of Laxogenin C on Increasing the Resistance to Drought Stress of Tobacco Seedlings [J]. Journal of Agricultural Science and Technology, 2018, 20(12): 36-44.
[2]	YANG Zhengtao1§, XIN Shurong1§, WANG Xingjie2, ZHANG Changai1*. Research Advance on the Application of Chitin Fertilizer [J]. Journal of Agricultural Science and Technology, 2018, 20(1): 130-136.
[3]	XIE Zheng-wen1, WANG Lian-jun2, CHEN Jin-yang1, WANG Jiao1, SU Yi-jun1, . Studies on WRKY Transcription Factors and Their Biological Functions in Plants [J]. Journal of Agricultural Science and Technology, 2016, 18(3): 46-54.
[4]	LI Yuan-yuan1,2, CAO Qing-he1,2*. Mechanism of Brassinosteroid Involved in Regulating Plant Development, Stress Resistance and its Application in Breeding [J]. , 2015, 17(2): 25-32.
[5]	ZHANG Shao-xuan1, LI Zhe2, LIU Xin1*, HUANG Rong-feng2. Expression Character of Rice SUPERNUMERARY BRACT (OsSNB) in Response to Abiotic Stress and Hormone [J]. , 2015, 17(1): 42-48.
[6]	ZHENG Jie, WANG Lei*. Advance in Mechanism of Brassinosteroids in \|Plant Development [J]. , 2014, 16(1): 52-58.
[7]	MO Xiao-ting, ZHAO Jun, FAN Yun-liu, WANG Lei. Research Progress on Structure and Function of Maize Transcription Factors [J]. , 2013, 15(3): 7-17.
[8]	WU Mao-sen, LI Lei, WU Jing, CHEN Hua-min, HE Chen-yang. Effects of Overexpression and RNAi-mediated Silence of OsCtBP-A Gene on Root Growth and Stress Resistance in Rice [J]. , 2010, 12(1): 106-110.