2022, Vol. 38中国科学院微生物研究所、中国微生物学会主办
文章信息
- 王黎明, 杨瑞珍, 孙加强
- WANG Liming, YANG Ruizhen, SUN Jiaqiang
- 油菜素内酯调控作物农艺性状和非生物胁迫响应的研究进展
- Regulation of crop agronomic traits and abiotic stress responses by brassinosteroids: a review
- 生物工程学报, 2022, 38(1): 34-49
- Chinese Journal of Biotechnology, 2022, 38(1): 34-49
- 10.13345/j.cjb.210236
-
文章历史
- Received: March 21, 2021
- Accepted: June 1, 2021
- Published: June 11, 2021
引用本文
|
2. 中国农业科学院作物科学研究所 农作物基因资源与基因改良国家重大科学工程, 北京 100081
2. National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China
全球人口增长、城市化、环境变化和新冠肺炎疫情所带来的一系列挑战，对全世界粮食产量提出了新的要求，而改善株型为提高作物产量提供了新思路。作物株型的决定因素包括株高、叶夹角、分蘖角度、分蘖数和穗型等农艺性状，它们与作物的光合效率、胁迫响应、籽粒产量和籽粒品质息息相关[1]。
株高(plant height, PHT) 是作物株型的主要决定因素之一，同时也是重要的农艺性状，与作物的收获指数和增产潜力直接相关，植株矮化有利于增强植物抗倒伏耐肥能力，从而提高作物产量[2-4]。分蘖角度和叶夹角也是株型的重要决定因素，适当的分蘖角度和叶夹角有利于提高作物的光合效率和抗倒伏能力，进而提高单株产量和收获指数[5]。同时，分蘖角度和叶夹角直接决定作物的种植密度，对田间群体产量的影响更大[5-7]。此外，分蘖数和穗型也直接决定作物产量[8-9]。作物株型受内源激素和环境因子的协同调控，植物激素包括生长素(auxin)、脱落酸(abscisic acid, ABA)、茉莉酸(jasmonic acid, JA)、赤霉素(gibberellic acid, GA)、细胞分裂素(cytokinin, CK)、乙烯(ethylene, ET)、独脚金内酯(strigolactones, SLs) 和油菜素内酯(brassinosteroid, BR) 等[10-16]；环境因子主要有光、温度、水分、养分和种植密度[1]。其中，BR是一类广泛分布于植物界的多羟化甾醇激素，能够调控细胞伸长、分裂和分化，在植物生长发育中起重要作用[17-19]。BR信号转导缺陷的突变体表现出矮化、叶片卷曲、在暗条件下生长下胚轴变短以及开花延迟等表型[20-21]。目前已有许多文章总结了BR的生物合成、信号转导、组织特异性功能和胁迫响应。然而，在这篇综述中，我们主要关注BR的生物合成和信号转导是如何调控水稻、小麦、玉米等主要作物株型发育的。
植物由于无法移动，经常会遇到各种生物和非生物胁迫，包括各种病原体、高温、低温、干旱和高盐等。其中，低温是一种主要的非生物胁迫，严重威胁植物的生长发育。为了应对这一不利的环境信号，植物进化出了一系列复杂的机制来应对，提高了它们承受冷胁迫的能力。在过去的10年中，植物对冷胁迫适应分子机制的研究取得了重大进展，包括冷胁迫传感器、蛋白激酶和转录因子等冷胁迫信号通路的关键组分被鉴定，研究还发现植物激素对冷胁迫的响应也存在重要的调控作用。因此，本文着重对BR调控植物冷信号通路的研究进展进行综述。此外，盐胁迫也是限制植物生长和生产力的主要非生物胁迫类型，可导致植物发生离子胁迫、渗透胁迫和二次胁迫，尤其是氧化胁迫。为了适应盐胁迫，植物依靠多种信号通路重新建立细胞内的离子、渗透和活性氧(reactive oxygen species, ROS) 稳态，其中包括BR信号通路。因此，本文也对BR信号调控植物对盐胁迫响应的研究进展进行综述。
1 BR的合成、降解以及信号转导截至目前，已从植物中分离出多种BRs，它们大多是具有生物活性的BRs的生物合成中间体和分解代谢产物，如芸苔素内酯(brassinolide, BL) 和栗甾酮(castasterone, CS)。与其他植物类固醇类似，BL由一种常见的甾醇前体-环阿屯醇(cycloartenol) 合成[17]，经过甲基化、还原反应和去饱和等一系列化学反应后，就会形成BR特异性前体菜油甾醇(campesterol, CR)。从BL到CR的步骤被称为BR的生物合成途径。目前已知的催化BR合成的酶包括还原酶DE-ETIOLATED2 (DET2) 和多种细胞色素P450，包括CONSTITUTIVE PHOTOMORPHOGENESIS AND DWARFISM (CPD)、DWARF4 (DWF4)、ROTUNDIFOLIA3 (ROT3)、CYP90D1、BRASSINOSTEROID-6-OXIDASES 1 (BR6ox1) 和BR6ox2[22-29]。编码这些酶的基因通过负反馈调节进行转录调控，以维持BR的内源稳态[30-31]。这些基因的表达还受其他调控因子的调控，转录共调控因子BREVIS RADIX (BRX) 可以调控CPD的表达，basic helix-loop-helix (bHLH) 转录因子CESTA是CPD的正调控因子[32-33]。DWF4编码BR生物合成过程中的一个限速酶，可被2种bHLH转录因子PHYTOCHRO ME INTERACTING FACTOR 4 (PIF4) 和TEOSI NTE BRANCHED1/ CYCLOIDEA/PROLIFERATI NG CELL FACTOR1 (TCP1) 调控[34-35]。研究表明，PIF4的蛋白积累和转录活性受光和温度的调控，从而将外源环境与内源BR水平偶联起来[36-38]。此外，BRs的生物活性也由BL和CS的分解代谢修饰决定，如细胞色素P450 PHYBAC TIVATION-TAGGED SUPPRESSOR1 (BAS1) 会催化C-26羟基化；UDP-糖基转移酶UGT73C5会催化23-O糖基化等[39-40]。
目前BR信号通路已经研究得比较清楚了。研究表明，拟南芥细胞表面有3个BR受体，分别为BRASSINOSTEROID-INSENSITIVE 1 (BRI1)、BRI1-LIKE 1 (BRL1) 和BRL3[41-42]。与BRs结合会触发BRI1与其共受体BRI1-associated-kinase 1 (BAK1) 形成异源二聚体并被反式磷酸化，导致2种蛋白都被激活。如图 1所示，当BR水平较高时，磷酸化的BRI1和BAK1蛋白会起始后续的磷酸化级联反应，从类受体蛋白激酶BRI1 substrate kinase 1 (BSK1) 和constitutive differential growth 1/CDG-like (CDG1/CDL) 到下游的BRI1 suppressor 1 (BSU1) 和BSU1-like (BSL) 磷酸酶[43-45]。接下来，BSU1/BSLs会使BRASSINOSTEROID-INSEN SITIVE 2 (BIN2)发生去磷酸化，从而使其失活[46]。泛素-蛋白酶体系统参与去磷酸化的BIN2的降解，使其下游转录因子brassinazole resistant 1 (BZR1) 和BR- insensitive-EMS-suppressor 1 (BES1)/BZR2去磷酸化[47-48]。此外，蛋白磷酸酶2A (PP2A) 也会介导BES1和BZR1的去磷酸化和激活[49-50]。去磷酸化的转录因子BZR1和BES1在细胞核内积累会直接激活下游BR响应基因的表达[31, 51]。
当BR水平较低时，BRI1的位点会被BRI1 KINASE INHIBITOR 1 (BKI1) 占据，抑制了BRI1与BAK1的相互作用[52]。随后的磷酸化级联被关闭，BSU1/BSLs发生去磷酸化并失活，导致BIN2被磷酸化并活化。被激活的BIN2使转录因子BZR1和BES1磷酸化不仅抑制了它们的活性，而且促进了它们与14-3-3蛋白的结合，从而抑制了它们的核定位[53]。此外，胞质中磷酸化的BZR1和BES1会被泛素-蛋白酶体系统(ubiquitin proteasome system, UPS) 降解，从而关闭BR信号[49]。总之，BR信号通路关键组分的活性和稳定性受磷酸化/去磷酸化和泛素化调控，此为BR信号转导的核心调控机制。
2 BR调控重要农艺性状的分子机制 2.1 BR调控株高的分子机制株高(PHT) 是作物株型的主要决定因素之一，同时也是重要的农艺性状，与收获指数和增产潜力直接相关。自20世纪60年代以来，“绿色革命”基因Reduced height1 (Rht-B1b) 和Rht2 (Rht-D1b) 的利用，显著提高了小麦的抗倒伏和耐高肥水能力，使小麦产量大幅提高[54]。小麦矮秆基因Rht1和Rht2编码的DELLA蛋白为GA信号通路的负调控因子，由于其N端的单碱基突变，导致DELLA蛋白更加稳定，从而引起小麦植株半矮化，施加外源GA也不能恢复其半矮化表型[54]。有研究表明，Rht-D1、Rht-B1和Rht24也为小麦育种中重要的“矮秆基因”[2-3]。以大麦dwarf突变体和小麦dwarf Rht-B1c Della突变体为背景，筛选到的“过度生长”突变体表现出不同程度的生长恢复表型，但恢复程度取决于GA生物合成能力、GA受体功能和DELLA蛋白活性，这说明植物体内GA信号的强度是株高的直接决定因素[55-56]。同样，水稻株高调控的关键基因大多与GA和BR等激素的生物合成和信号转导途径有关[16, 57]。
GA信号的负调控因子DELLAs通过与BR信号的核心转录因子BZR1相互作用来抑制BZR1的DNA结合活性，而GA促进DELLA的降解会增强BR信号[58-59]。因此，BZR1- DELLAs相互作用被认为是BR和GA信号通路之间的交互点。最近的研究表明，BR能通过调控GA的生物合成来调节细胞伸长，BR相关突变体的内源GA水平以及GA代谢基因GA20ox-2、GA3ox-2、GA2ox-3等的表达水平发生了变化，同时GA3ox-2突变体对BR的敏感性降低[57, 60-61]。OsBZR1能与3个GA代谢基因启动子直接结合说明GA生物合成是BR信号下游通路之一[60]。
BR的生物学功能存在剂量效应，高浓度BR会抑制GA的合成[60]，这可能是高浓度BR抑制植物生长、BR敏感性增强的水稻植株矮化的直接原因。BR的这种剂量效应是通过诱导和招募负调控转录因子来实现的。研究表明，BR信号的核心负调控因子GLYCOGEN SYNTHASE KINASE2 (GSK2) 能通过与GRAS家族蛋白DWARF AND LOW-TILLERING (DLT) 相互作用来调控植物对BR的响应[62]。此外，Ovate Family Protein 1 (OFP1) 与DLT之间也存在相互作用。OsOFP1过表达植株与OsDLT过表达植株表型类似，且OFP1对植物株型的调控依赖于DLT的功能。BR处理会诱导OFP1的表达，BR信号的关键转录因子OsBZR1能结合OFP1的启动子。此外，OFP1过表达植株BR信号增强使得GA的合成被抑制，表现出株高降低的表型[63]。GAMYBL2会抑制GA合成基因CPS1和GA3ox-2的表达，BR和GA均能诱导GAMYBL2降解来促进GA合成[64]。BR还能通过OsBZR1诱导miR396d表达来抑制OsGRF6的表达，进而抑制GA的生物合成和信号转导[65]。GYMYBL2和miR396d过表达会导致作物矮化[64-65]。综上所述，BR能通过多种途径来调节GA水平进而调控作物株高。OsBAK1 (拟南芥BAK1的同源基因) 编码SERK家族受体激酶蛋白，作为OsBRI1的共受体介导BR信号转导，它对水稻株高有调控作用。OsBAK1过表达植株株高显著降低[66]。此外，笔者的研究还发现，小麦中的blue-light inhibitor of cryptochromes 1 (TaBIC1) 可以作为TaBZR1的转录共激活因子来精细调控小麦株高[67]。
2.2 BR调控叶夹角的分子机制叶夹角(leaf angle, LA) 是指植物叶片中脉与垂直茎之间的倾斜度。叶夹角特别是旗叶夹角是水稻理想植株的主要组成部分，在田间会影响光源获取和相邻植物之间的竞争，对水稻籽粒产量贡献较大[68]。具有直立叶性状的植株可以密集种植，因此培育直立叶水稻新品种是提高水稻产量的关键策略。研究表明，植物激素通过协调其生物合成和信号转导广泛参与LA的调控，BR在其中起主导作用。
在叶节(lamina joint) 处喷施BR或通过促进BR相关调控因子的表达，增强BR信号会导致LA的增加，说明BR是LA的正调控因子[69]。许多研究表明，水稻LA与BR的生物合成或信号转导密切相关，BR生物合成基因如Dwarf2 (D2)功能缺失会使内源BR水平降低，最终导致叶片直立表型[70-71]。此外，其他BR生物合成调控因子，如细胞色素P450家族蛋白，也在LA的调控中发挥重要作用。例如，BR-deficient Dwarf1 (OsBRD1) 编码催化BR生物合成的关键酶(BR C-6氧化酶)，OsBRD1突变会导致水稻严重的缺陷，包括植株矮化、叶片扭曲、穗变短以及籽粒变小等[72-73]。另外2个细胞色素P450蛋白Osdwarf4和Osdwarf11也可以催化BR生物合成的限速反应(c-22羟基化)。Osdwarf4在水稻叶片中高表达，BR抑制了Osdwarf4的表达，在BR不敏感或缺陷突变体中Osdwarf4的表达增加，说明存在反馈调节作用。与野生型植株相比，Osdwarf4突变体出现叶片直立的表型，但叶片、穗和籽粒的发育不受影响[70]。与Osdwarf4突变体相比，Osdwarf11突变体表现出更严重的表型，包括植株矮化、叶片直立、花粉败育和籽粒变小。进一步研究发现，Osdwarf4和Osdwarf11在BRs生物合成中均存在冗余作用，但Osdwarf11在BR生物合成途径中发挥主要作用，Osdwarf4发挥互补作用[74]，这可能也是Osdwarf4和Osdwarf11表型差异较大的原因。综上所述，BR的合成和代谢在作物LA的调控中发挥至关重要的作用。
除上述BR生物合成基因外，BR信号转导基因在调控水稻LA中也发挥着重要作用。例如水稻OsBRI1是拟南芥BRI1的同源蛋白，OsBRI1参与调节水稻生长发育的多个过程，包括叶夹角、居间分生组织的形成和节间细胞的纵向伸长。水稻OsBRI1连锁基因DWARF61 (D61) 突变体d61由于叶枕发育受损，表现出叶片直立生长的表型[75]。水稻OsBAK1的表达水平降低会出现叶片直立的表型，且水稻繁殖不受影响，因此被认为是提高水稻产量的一个基因资源[66]。此外，水稻OsBZR1的RNAi植株出现矮化和叶片直立的表型，说明BR信号下游核心转录因子OsBZR1在调控水稻LA中也起重要作用[76]。研究表明，水稻14-3-3蛋白与OsBZR1在细胞质中存在相互作用，最终抑制其入核发挥转录因子的作用。而BR处理可以打破它们之间的相互作用，激活OsBZR1的表达，从而导致叶夹角增大的表型[76-77]。水稻Zinc finger转录因子LEAF and TILLER ANGLE INCREASED CONTROLLER (OsLIC) 通过直接调节叶夹角的正调控因子INCREASED LEAF INCLINATION 1 (ILI1) 来拮抗OsBZR1，抑制水稻BR信号转导。过表达OsLIC植物体BR信号减弱，出现叶片直立的表型，说明OsLIC1是水稻叶片角度的负调控因子[77]。此外，还有研究表明，APETALA2(AP2)/ethylene-responsive element binding factor (ERF) 家族转录因子reduced leaf angle 1 (RLA1)/small organ size 1 (SMOS1) 通过与OsBZR1相互作用来增强其转录活性，从而增强BR信号，使水稻的LA增加[78-79]。BRASSINOSTER OID UPREGULATED1 (BU1) 编码helix-loop-helix蛋白，是BR信号的正调控因子。水稻中BU1过表达导致叶夹角增大、籽粒增大，而水稻BU1-RNAi株系出现叶片直立的表型[80]。此外，一对HLH/bHLH拮抗因子OsILI1 (拟南芥Paclobutrazol Resistance 1 (PRE1)) 的同源蛋白和ILI1 binding bHLH 1 (OsIBH1)，在OsBZR1下游起调控水稻叶夹角的作用。OsILI1正向调节BR介导的细胞伸长，OsIBH1直接与OsILI1相互作用，发挥相反的作用[81]。此外，另一种bHLH转录因子BRASSINOSTEROID-RESPONSIVE LEAF ANGLE REGULATOR 1 (OsBLR1) 也通过BR途径参与调控水稻的LA。过表达OsBLR1会同时出现LA变大、粒长增加以及对BR的敏感增加，而OsBLR1突变体出现叶片直立、粒长变短的表型[82]。同样，水稻OsbHLH079的功能获得突变体也出现LA变大、粒长增加以及对BR的敏感增加的表型，OsbHLH079-RNAi则表现出相反的表型[83]。转录因子OsWRKY53是水稻BR信号的正调控因子，oswrky53突变体的叶片直立，而OsWRKY53过表达植株表现出叶夹角增大的表型[84]。总之，这些研究表明BR信号转导的调控因子广泛参与对水稻LA调控。
2.3 BR调控花器官的分子机制BRs是植物特有的类固醇激素，除了在细胞伸长和应激响应中的作用以外，BRs的时空分布模式也会影响植物花器官的发生与发育[85]。研究发现，在拟南芥BR缺陷突变体和组成型突变体中器官边界的形成发生了改变。BR信号下游TFsBZR1/BES1可以招募抑制子TOPLESS (TPL) 来抑制植物器官边界识别基因cup shaped cotyledon 1 (CUC1)、CUC2、CUC3、lateral ORGAN fusion1和lateral organ boundaries (LOB) 的表达[86]。此外，LOB激活了PHYB ACTIVATION TAGGED SUPPRESSOR1 (BAS1) 的表达，它编码细胞色素P450，能抑制BRs活性，从而形成负反馈环来限制器官边界区域的生长[87]。同时，水稻BRs缺陷突变体panicle morphology mutant 1 (pmm1) 出现了丛生的花序和成对的小穗[88]。此外，BR生物合成和信号转导突变体，如dwarf 11 (d11) 和bri1-associated receptor kinase (Osbak1)/Ossg2突变体的小穗数量也发生了变化[89-91]。在一些水稻品种中，FZP启动子区中存在2个CGTG基序，OsBZR1通过结合CGTG基序抑制FZP的表达，使得SpM向FM的转换时间延长，导致小穗数量增加[92]。因此，通过改变FZP启动子CGTG基序的数量来改变BZR1-FZP调控模块，可以作为水稻育种工作的切入点。
在拟南芥中，flower meristem (FM) 的组分LFY可以抑制GA的生物合成，从而影响细胞分裂和伸长[93]。LFY激活EUI-like P450 A1 (ELA1) 的表达，它编码细胞色素酶P450，将有生物活性的GAs降解[94]。与此同时，DELLAs蛋白水平升高，并与SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 9 (SPL9) 相互作用，进而激活AP1的表达，强化FM的身份[95-96]。此外，对拟南芥和大麦的研究发现，DELLAs的积累抑制IM的大小[97]，这表明GA的时空分布影响花的数量和开花时间，进而影响产量。然而，拟南芥的LFY-ELA1-SPL9-AP1调控元件是否在其他禾谷类作物中对小穗和小花的形成有类似的作用尚不清楚。因此，进一步探究植物激素在花序生殖分生组织转化过程中的时空分布规律及其下游靶点对于作物育种具有重要意义。
2.4 BR调控穗型和籽粒大小的分子机制如前文所述，株高、分蘖数、分蘖角度、叶型和叶夹角都是决定作物产量的重要因素，但它们都是间接影响作物产量。而穗型和籽粒大小是直接决定作物产量的重要农艺性状，二者同样是由植物激素和外源环境协同调控的，BR的生物合成与代谢、信号转导在其中发挥着至关重要的作用。
研究表明，CLUSTERED PRIMARYBRANCH 1 (CPB1)基因是DWARF11 (D11) 的等位基因，编码细胞色素P450蛋白，参与BR生物合成途径。遗传转化实验证明位于CPB1/D11高度保守区域的His360Leu氨基酸替换是导致cpb1突变体穗型和籽粒大小变化的原因。在cpb1突变体背景下过表达CPB1/D11，不仅能恢复正常的穗型和株高，而且叶角度和籽粒大小也大于野生型。此外，通过穗特异性启动子驱动的CPB1/D11转基因植株可以在不影响其他有利农艺性状的基础上增加籽粒大小，提高作物产量[89]。此后又发现Notched Belly Grain 4 (NBG4) 也是DWARF11 (D11) 的新等位基因，NBG4能通过调节OsPPS-2、OsPRA2、OsYUCCA1、sped1-D和Dwarf的表达来最终调控作物的穗型和粒型[98]。这些结果表明，BR生物合成的调控因子CPB1/D11/NBG4能够调节穗型和籽粒大小，是提高作物产量的优异基因资源。
OsBAK1除了调控水稻的株高、叶角度外，还影响籽粒大小。OsBAK1过表达植株粒重变小[66]。Top Bending Panicle1 (TBP1) 是参与BR信号转导的体细胞胚胎发生受体激酶(Somatic embryogenesis receptor kinases，SERKs) 家族的成员，tbp1突变体植株矮化，叶片直立，籽粒小而圆，分蘖增多，穗更短更密[99]。DS1/ OsEMF1与OsARF11相互作用共同调节OsBRI1的表达，ds1突变改变了BR信号相关基因的表达，对BL处理不敏感。ds1突变体表现出株高降低、籽粒变小和叶角度变小的表型[100]。新发现的BRD2等位基因Longer Top Branch and Shorter Grain 1 (LTBSG1) 能通过影响BR生物合成调控水稻穗型和籽粒发育[101]。此外，前文提到的BR信号正调控因子OsbHLH079也与水稻粒型有关，其T-DNA插入突变体osbhlh079-D中BR信号相关基因的表达显著上调，同时对外源BR敏感。OsbHLH079过表达植株和osbhlh079-D突变体表型相似，粒长都增加，而其RNAi植株表现出相反的表型[83]。同时，BU1也能正调控水稻籽粒大小[80]。最近的研究表明，玉米转录因子ZmBES1/BZR1-5也能正调控籽粒大小[102]。转录因子OsWRKY53是水稻BR信号的正调控因子，oswrky53突变体的籽粒变小，而OsWRKY53过表达植株籽粒增大[84]。总之，这些研究表明BR信号正调控因子对水稻籽粒有积极的调控作用。
此外，转录因子OFP1与GSK2蛋白激酶存在相互作用，抑制GSK2激酶活性可显著促进OFP1蛋白的积累。除叶片变窄、叶角度增大、株高降低和分蘖数减少外，OFP1过表达植株籽粒变得长而窄[63]。OsOFP19通过与Dwarf and Low-Tillering (DLT) 和Oryza Sativa Homeobox1 (OSH1) 相互作用负调控BR反应，并将其与细胞分裂模式整合，影响作物的株型和粒型。过表达OsOFP19会使皮下组织细胞层增加，从而导致株高降低、叶片变厚。进一步的研究发现，OsOFP19与OSH1相互作用，这种相互作用增强了两者的转录活性，导致细胞从背斜分裂向周周分裂过渡。此外，DLT能同时与OsOFP19和OSH1相互作用，并在这两种相互作用中起到拮抗剂的作用。因此，OsOFP19、OSH1和DLT通过形成功能复合体，在调节BR信号转导和调控作物株型等方面发挥关键作用[103]。OFP3在BR响应中起负调控作用，最新的研究表明，OVATE FAMILY PROTEIN 3 (OFP3) 能与GSK2和DLT相互作用，敲除OFP3促进了水稻幼苗的生长，但过表达OFP3导致对BR不敏感，水稻株高降低、叶夹角和籽粒都变小。有趣的是，BR生物合成基因和信号转导基因在OFP3过表达植物中的表达都降低。OFP3能与自身以及其他BR信号相关成员(包括OFP1、OSH1、OSH15、OsBZR1和GF14c) 相互作用。重要的是，GSK2可以磷酸化OFP3并增强这些相互作用。OFP3作为BR合成和信号转导的抑制因子，能被GSK2稳定后将其整合到转录因子复合物中，以促进对BR信号转导的控制，这对水稻株型和粒型的调控是至关重要的[104]。
3 BR与抗逆由于植物不能移动，它们必须调整自身的生长和发育以承受环境压力，如冷胁迫和盐胁迫[105-106]。植物生长和应激反应通常是相互拮抗的，因此需要平衡[107]。研究表明，植物激素BR在植物响应非生物胁迫中起正向调控作用，外源喷施一定浓度的BR会增强作物对冷冻胁迫和盐胁迫的耐受性。
3.1 BR与冷胁迫冷胁迫是限制植物生长、发育和地理分布的主要环境因子，包括低温胁迫(0–15 ℃) 和冻胁迫(< 0 ℃)，它们都会对植物造成严重的损害[108]。植物在进化过程中形成了一系列的冷胁迫响应机制，解析植物对冷胁迫的响应机制，有助于培育耐寒的作物品种。研究表明，转录因子C-REPEAT BINDING FACTOR/DRE BINDING FACTOR1 (CBF/DREB1) 在冷胁迫响应中至关重要。CBF转录因子能直接激活一系列冷调控基因(COR)，提高植物抗冻能力[109-110]。模式植物拟南芥冷处理后15–30 min内，CBF基因的表达被强烈诱导，在1–3 h表达达到高峰，随后迅速下降[111]。因此，CBF基因在冷胁迫前、冷胁迫开始、冷胁迫减弱3个阶段有不同的表达模式[112]。冷胁迫下，CBF的表达受多种转录因子的调控[108]。其中，INDUCER OF CBF EXPRESSION (ICE1) 和钙调蛋白结合转录激活因子在CBF上游正调控其表达[113-115]；反过来，MYB15、ETHYLENE INSENSITI VE3、PHYTOCHROME-INTERACTING FACTOR3 (PIF3)、PIF4和PIF7是CBF的负调控因子[108, 116-117]。总之，CBF的表达是受精确调控的。
研究表明，蛋白激酶能够调控植物对冷胁迫的响应[108, 118]。SNF1相关蛋白激酶家族成员OPENSTOMATA1 (OST1) 能够正调控植物对冷胁迫的响应[119-120]。蛋白磷酸酶cladee growth- regulating2是冷胁迫激活OST1的关键调节因子[121]。低温激活的OST1使ICE1磷酸化，并减弱其与E3泛素连接酶high expression of osmotically responsive gene1 (HOS1) 的相互作用，增强ICE1的稳定性，从而提高植物的抗冻能力[119]。此外，OST1磷酸化肌肽相关复合物的β亚基-BASIC TRANSCRIPTION FACTOR3蛋白，并促进其与CBF蛋白的相互作用，从而增强CBF蛋白的稳定性[120]。模式植物拟南芥在响应冷胁迫过程中，MITOGEN-ACTIVATED PROTEIN KINASE3 (MPK3) 和MPK6能够磷酸化并降解ICE1[112, 122]。但在水稻中存在不同的机制，OsMPK3磷酸化OsICE1并破坏OsICE1- OsHOS1之间的相互作用，从而稳定ICE1[123]。除了MPK3和MPK6之外，位于质膜上的类受体COLD-RESP ONSIVE PROTEIN KINASE1是冷信号通路的负调控因子。冷胁迫激活的COLD-RESPONSIVE PROTEIN KINASE1磷酸化14-3-3蛋白，促进它们从细胞质进入细胞核，与CBF蛋白相互作用并使其不稳定，从而降低植物的抗冻性[105, 124]。
MPK3和MPK6能磷酸化ICE1的Ser94位点[112, 122]，但不影响ICE1和E3连接酶HOS1之间的相互作用[122]，而BIN2增强了它们的相互作用，且ICE1的Ser94位点介导了这种增强[125]。因此，这些蛋白激酶作用于ICE1的机制不同。MPK3和MPK6在冷胁迫响应的早期被激活，并首先磷酸化ICE1[112, 122]。最新的研究发现，BIN2与转录因子ICE1相互作用并使其磷酸化，促进ICE1与HOS1相互作用，加速HOS1介导的ICE1降解，从而下调CBF基因的表达[125]。在低温环境(4 ℃处理1 h) 下，植物BIN2的激酶活性显著下降，随后恢复(4 ℃处理2 h后)；在4 ℃处理3 h后，BIN2会使ICE1的蛋白水平降低。BIN2能分别通过转录因子ICE1、BZR1和CESTA负调控CBF基因的表达。因此，冷胁迫会释放BIN2介导的对转录因子ICE1、BZR1和CESTAs的抑制作用。这一过程使CBF基因在冷胁迫响应的早期得到最大程度的诱导，从而提高植物的抗冻能力。同时，冷胁迫也抑制了这些转录因子的活性，确保在冷胁迫衰减期CBF能被控制在适当的表达水平。这些结果表明，BIN2促进了ICE1的降解，主要发生在冷胁迫响应中CBF基因表达减弱的阶段，从而平衡了植物生长和冷胁迫响应[125]。
BR信号的核心转录因子BZR1作用于CBF1和CBF2上游部分调控两者的表达，进而诱导CBF调节子的表达。此外，BZR1也可以调节独立于CBF的COR基因的表达，包括WRKY6、PYL6、SOC1、SAG21和JMT。BIN2负调控BZR1对冷胁迫的响应，而冷胁迫诱导的BZR1去磷酸化水平与植物的耐寒性相关。总之，BZR1能以CBF依赖和CBF不依赖的方式正向调节植物对冷胁迫的响应[126]。
3.2 BR与盐胁迫大多数作物受到的土壤盐分胁迫比干旱或温度胁迫时间要长。当土壤盐分随降雨或灌溉而降低时，植物必须从盐胁迫反应阶段转入快速生长恢复阶段。BIN2-SOS3/SCaBP8-SOS2模块在生长恢复阶段发挥作用，调节植物从盐胁迫响应向快速生长的过渡。BIN2与钙传感器SOS3和SCaBP8协同调节BR调控的植物生长和SOS通路介导的盐胁迫响应[127]。在正常情况下，BR信号通过促进BIN2的质膜定位和BZR1/BES1家族转录因子的转录活性来促进植物生长。在盐胁迫下，SOS3和SCaBP8能够感知并解码盐诱导的钙信号，并将SOS2招募到质膜，使其磷酸化并激活SOS1。随后，BIN2与质膜分离，磷酸化并抑制BZR1/BES1的转录活性，抑制植物生长。BIN2还可以抑制SOS2的活性，避免其过度激活。盐胁迫可能会诱导其他调控因子进一步抑制植物生长。在盐胁迫后的快速恢复阶段，SOS3和SCaBP8可能感知到钙信号的改变，进而促进BIN2进入质膜，强烈抑制SOS2活性，也抑制了对SOS2的依赖植物的胁迫反应；BZR1/BES1的转录活性增强，促进植物生长恢复[127]。
研究表明，不同的GSK3类激酶能通过磷酸化不同的蛋白质来调控不同的非生物胁迫响应[125, 128-129]。盐胁迫下，BIN2通过SOS途径负调控主根生长。BIN2作为一个限速调节因子，可以避免盐胁迫下SOS2的过度激活，同时作为一个抑制因子，可以在盐胁迫后的恢复期通过SOS3和SCaBP8抑制SOS2的活性[127]。BIN2以典型的GSK3类激酶识别基序磷酸化SOS2的T169位点和激活环上的T172残基。这些残基在SOS2类蛋白激酶(PKS/CIPK) 家族成员中高度保守[130]。GSK3类激酶调节植物的发育、生长和应激反应，而BIN2、BIL1和BIL2激酶的缺失影响其他附加途径[131]。例如，GSK3类激酶在BR与其他激素信号(如ABA、GA、生长素) 的相互作用中发挥重要作用，可能会影响初生根的生长[132-134]。
研究表明，AtSOS2和人AMP-activated PKS catalytic subunit α1 (AMPKα1) 激酶结构域的蛋白序列相似度超过40%，而AtBIN2和人GSK3β整个蛋白序列的相似度约为60%。GSK-3β在合成代谢环境中能磷酸化并抑制AMPKα1[135]，而在植物盐胁迫响应中，BIN2磷酸化并抑制SOS2[127]，这表明这些蛋白在动物和植物对环境变化的反应中可能具有相似的调节机制。在动物体内，GSK3的催化功能是通过启动磷酸化或与支架蛋白的相互作用来实现的，而这些启动步骤对于植物GSK3类激酶来说并不是必需的[19, 131]。SOS3和SCaBP8显著增强了SOS2和BIN2之间的相互作用和磷酸化，说明SOS3和SCaBP8作为连接SOS2和BIN2的支架蛋白[127]。SOS3和SCaBP8是钙结合蛋白，参与负调控特定盐胁迫诱导的钙信号[136]。通过抑制盐胁迫诱导的钙信号使BIN2和SOS3/SCaBP8的解离消失[127]，说明钙信号可能在盐胁迫恢复阶段发生变化；而SOS3/SCaBP8能促进BIN2进入质膜来抑制SOS2活性[127]，这说明在盐胁迫后的恢复阶段，SOS3和SCaBP8对BIN2的识别以及BIN2-SOS3/SCaBP8-SOS2复合物的形成依赖于钙信号和高的SOS2活性。
BIN2磷酸化BZR1/BES1会介导其降解[49]。盐胁迫下BES1的稳定性和磷酸化状态受到了调节[127]。之前的研究表明，BZR1/BES1能结合到DWF4的启动子上抑制其表达，从而形成BR合成的负反馈调控环[49, 137]。在盐胁迫后的恢复阶段，BIN2被SOS3和SCaBP8固定在质膜上，BZR1/BES1被释放，导致DWF4表达下降。
以往的研究表明，BR信号是植物响应盐胁迫必需的[138-139]。最新的研究也表明，在盐胁迫下GSK3类激酶能抑制植物初生根的生长，而部分BR信号突变体的盐敏感性和SOS2活性与野生型无明显差异[127]，说明盐胁迫下GSK3类激酶调控的SOS通路部分独立于BR信号。盐胁迫响应是一个时空调控过程，包括钙信号、活性氧(ROS) 信号、多种植物激素信号和转录调控[13, 140-141]。除了SOS信号通路外，BR信号还可能参与植物抗盐胁迫的其他调控机制。
4 总结与展望BRs在植物整个生命周期中具有非常广泛的作用。然而，现有证据表明内源BRs不经过长途运输。因此，在特异组织或器官水平上调控BR生物合成、分解代谢和信号转导对优化植物生长以响应不同发育阶段和环境变化至关重要。虽然已经发现了许多内在遗传因子能调控BR的生物合成和信号转导，但关于这些遗传因子如何与特定发育阶段或不同外界环境因素整合的分子机制还不清楚。
作物株型的决定因素包括株高、叶夹角、分蘖角度、分蘖数和穗型等农艺性状，它们与作物的光合效率、胁迫响应、籽粒产量和籽粒品质息息相关，也直接决定作物收获指数和增产潜力。BR的生物合成和信号转导对作物株型有重要的调控作用，笔者的研究表明，TaBIC1可以作为TaBZR1的转录共激活因子来精细调控小麦株高[67]；光信号受体CRY1可以通过抑制BZR1的DNA结合活性和促进其磷酸化来负调控BR信号转导，从而整合外界光信号与内源BR信号来协同调控植物株型。因此，可以通过对BR途径特异基因进行基因编辑或筛选优异等位变异，培育株型紧凑(提高群体光合效率)、高光效(叶色深绿) 的作物新种质。此外，笔者的研究还发现(另文发表)，BR信号关键组分与表观遗传因子整合来调控作物的抗逆性，探索盐胁迫、冷胁迫等非生物胁迫如何影响植物BR生物合成和信号转导的精确调控机制，将有助于通过基因编辑或分子设计育种来提高作物抗逆性。
| [1] |
Wang YH, Li JY. Molecular basis of plant architecture. Annu Rev Plant Biol, 2008, 59: 253-279. DOI:10.1146/annurev.arplant.59.032607.092902
|
| [2] |
Wurschum T, Langer SM, Longin CFH. Genetic control of plant height in European winter wheat cultivars. Theor Appl Genet, 2015, 128(5): 865-874. DOI:10.1007/s00122-015-2476-2
|
| [3] |
Tian XL, Wen WE, Xie L, et al. Molecular mapping of reduced plant height gene Rht24 in bread wheat. Front Plant Sci, 2017, 8: 1379. DOI:10.3389/fpls.2017.01379
|
| [4] |
Castorina G, Consonni G. The role of brassinosteroids in controlling plant height in Poaceae: a genetic perspective. Int J Mol Sci, 2020, 21(4): E1191. DOI:10.3390/ijms21041191
|
| [5] |
Sinclair TR, Sheehy JE. Erect leaves and photosynthesis in rice. Science, 1999, 283(5407): 1456.
|
| [6] |
Mantilla-Perez MB, Salas Fernandez MG. Differential manipulation of leaf angle throughout the canopy: current status and prospects. J Exp Bot, 2017, 68(21/22): 5699-5717.
|
| [7] |
Wang RN, Liu C, Li QZ, et al. Spatiotemporal resolved leaf angle establishment improves rice grain yield via controlling population density. iScience, 2020, 23(9): 101489. DOI:10.1016/j.isci.2020.101489
|
| [8] |
Chen GF, Wu RG, Li DM, et al. Genomewide association study for seeding emergence and tiller number using SNP markers in an elite winter wheat population. J Genet, 2017, 96(1): 177-186. DOI:10.1007/s12041-016-0731-1
|
| [9] |
Yuan Z, Persson S, Zhang DB. Molecular and genetic pathways for optimizing spikelet development and grain yield. aBIOTECH, 2020, 1(4): 276-292. DOI:10.1007/s42994-020-00026-x
|
| [10] |
Dai ZY, Wang J, Yang XF, et al. Modulation of plant architecture by the miR156f-OsSPL7-OsGH3.8 pathway in rice. J Exp Bot, 2018, 69(21): 5117-5130. DOI:10.1093/jxb/ery273
|
| [11] |
Wang JY, Wang RT, Mao XG, et al. TaARF4 genes are linked to root growth and plant height in wheat. Ann Bot, 2019, 124(6): 903-915. DOI:10.1093/aob/mcy218
|
| [12] |
Garrido AN, Supijono E, Boshara P, et al. Flasher, a novel mutation in a glucosinolate modifying enzyme, conditions changes in plant architecture and hormone homeostasis. Plant J, 2020, 103(6): 1989-2006. DOI:10.1111/tpj.14878
|
| [13] |
Chen YP, Dan ZW, Gao F, et al. Rice growth-regulating factor7 modulates plant architecture through regulating GA and indole-3-acetic acid metabolism. Plant Physiol, 2020, 184(1): 393-406. DOI:10.1104/pp.20.00302
|
| [14] |
Yin WC, Xiao YH, Niu M, et al. ARGONAUTE2 enhances grain length and salt tolerance by activating big grain3 to modulate cytokinin distribution in rice. Plant Cell, 2020, 32(7): 2292-2306. DOI:10.1105/tpc.19.00542
|
| [15] |
Zhou F, Lin QB, Zhu LH, et al. D14-SCF(D3)-dependent degradation of D53 regulates strigolactone signalling. Nature, 2013, 504(7480): 406-410. DOI:10.1038/nature12878
|
| [16] |
Tong HN, Chu CC. Functional specificities of brassinosteroid and potential utilization for crop improvement. Trends Plant Sci, 2018, 23(11): 1016-1028. DOI:10.1016/j.tplants.2018.08.007
|
| [17] |
Yokota T. The structure, biosynthesis and function of brassinosteroids. Trends Plant Sci, 1997, 2(4): 137-143. DOI:10.1016/S1360-1385(97)01017-0
|
| [18] |
Clouse SD, Sasse JM. Brassinosteroids: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol, 1998, 49(1): 427-451. DOI:10.1146/annurev.arplant.49.1.427
|
| [19] |
Nolan T, Chen JN, Yin YH. Cross-talk of brassinosteroid signaling in controlling growth and stress responses. Biochem J, 2017, 474(16): 2641-2661. DOI:10.1042/BCJ20160633
|
| [20] |
Wang ZY, Bai MY, Oh E, et al. Brassinosteroid signaling network and regulation of photomorphogenesis. Annu Rev Genet, 2012, 46: 701-724. DOI:10.1146/annurev-genet-102209-163450
|
| [21] |
Yang CJ, Zhang C, Lu YN, et al. The mechanisms of brassinosteroids' action: from signal transduction to plant development. Mol Plant, 2011, 4(4): 588-600. DOI:10.1093/mp/ssr020
|
| [22] |
Ohnishi T, Godza B, Watanabe B, et al. CYP90A1/CPD, a brassinosteroid biosynthetic cytochrome P450 of Arabidopsis, catalyzes C-3 oxidation. J Biol Chem, 2012, 287(37): 31551-31560. DOI:10.1074/jbc.M112.392720
|
| [23] |
Choe S, Dilkes BP, Fujioka S, et al. The DWF4 gene of Arabidopsis encodes a cytochrome P450 that mediates multiple 22α-hydroxylation steps in brassinosteroid biosynthesis. Plant Cell, 1998, 10(2): 231-243.
|
| [24] |
Fujita S, Ohnishi T, Watanabe B, et al. Arabidopsis CYP90B1 catalyses the early C-22 hydroxylation of C27, C28 and C29 sterols. Plant J, 2006, 45(5): 765-774. DOI:10.1111/j.1365-313X.2005.02639.x
|
| [25] |
Fujioka S, Takatsuto S, Yoshida S. An early C-22 oxidation branch in the brassinosteroid biosynthetic pathway. Plant Physiol, 2002, 130(2): 930-939. DOI:10.1104/pp.008722
|
| [26] |
Kim GT, Fujioka S, Kozuka T, et al. CYP90C1 and CYP90D1 are involved in different steps in the brassinosteroid biosynthesis pathway in Arabidopsis thaliana. Plant J, 2005, 41(5): 710-721. DOI:10.1111/j.1365-313X.2004.02330.x
|
| [27] |
Ohnishi T, Szatmari AM, Watanabe B, et al. C-23 hydroxylation by Arabidopsis CYP90C1 and CYP90D1 reveals a novel shortcut in brassinosteroid biosynthesis. Plant Cell, 2006, 18(11): 3275-3288. DOI:10.1105/tpc.106.045443
|
| [28] |
Kim TW, Hwang JY, Kim YS, et al. Arabidopsis CYP85A2, a cytochrome P450, mediates the Baeyer-Villiger oxidation of castasterone to brassinolide in brassinosteroid biosynthesis. Plant Cell, 2005, 17(8): 2397-2412. DOI:10.1105/tpc.105.033738
|
| [29] |
Kwon M, Fujioka S, Jeon JH, et al. A double mutant for the CYP85A1 and CYP85A2 genes of Arabidopsis exhibits a brassinosteroid dwarf phenotype. J Plant Biol, 2005, 48(2): 237-244. DOI:10.1007/BF03030413
|
| [30] |
Sun Y, Fan XY, Cao DM, et al. Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev Cell, 2010, 19(5): 765-777. DOI:10.1016/j.devcel.2010.10.010
|
| [31] |
Yu XF, Li L, Zola J, et al. A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J, 2011, 65(4): 634-646. DOI:10.1111/j.1365-313X.2010.04449.x
|
| [32] |
Mouchel CF, Osmont KS, Hardtke CS. BRX mediates feedback between brassinosteroid levels and auxin signalling in root growth. Nature, 2006, 443(7110): 458-461. DOI:10.1038/nature05130
|
| [33] |
Poppenberger B, Rozhon W, Khan M, et al. CESTA, a positive regulator of brassinosteroid biosynthesis. EMBO J, 2011, 30(6): 1149-1161. DOI:10.1038/emboj.2011.35
|
| [34] |
Wei ZY, Yuan T, Tarkowská D, et al. Brassinosteroid biosynthesis is modulated via a transcription factor cascade of COG1, PIF4, and PIF5. Plant Physiol, 2017, 174(2): 1260-1273. DOI:10.1104/pp.16.01778
|
| [35] |
Guo ZX, Fujioka S, Blancaflor EB, et al. TCP1 modulates brassinosteroid biosynthesis by regulating the expression of the key biosynthetic gene DWARF4 in Arabidopsis thaliana. Plant Cell, 2010, 22(4): 1161-1173. DOI:10.1105/tpc.109.069203
|
| [36] |
Koini MA, Alvey L, Allen T, et al. High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr Biol, 2009, 19(5): 408-413. DOI:10.1016/j.cub.2009.01.046
|
| [37] |
Oh E, Zhu JY, Wang ZY. Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat Cell Biol, 2012, 14(8): 802-809. DOI:10.1038/ncb2545
|
| [38] |
Kumar SV, Lucyshyn D, Jaeger KE, et al. Transcription factor PIF4 controls the thermosensory activation of flowering. Nature, 2012, 484(7393): 242-245. DOI:10.1038/nature10928
|
| [39] |
Poppenberger B, Fujioka S, Soeno K, et al. The UGT73C5 of Arabidopsis thaliana glucosylates brassinosteroids. PNAS, 2005, 102(42): 15253-15258. DOI:10.1073/pnas.0504279102
|
| [40] |
Neff MM, Nguyen SM, Malancharuvil EJ, et al. BAS1: a gene regulating brassinosteroid levels and light responsiveness in Arabidopsis. PNAS, 1999, 96(26): 15316-15323. DOI:10.1073/pnas.96.26.15316
|
| [41] |
Wang ZY, Seto H, Fujioka S, et al. BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature, 2001, 410(6826): 380-383. DOI:10.1038/35066597
|
| [42] |
Ca o-Delgado A, Yin Y, Yu C, et al. BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development, 2004, 131(21): 5341-5351. DOI:10.1242/dev.01403
|
| [43] |
Wang H, Wei Z, Li j, et al. Brassinosteroids: hormone metabolism and signaling in plants: the current model of BR signaling 2017: 299-308.
|
| [44] |
Li J, Wen J, Lease KA, et al. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell, 2002, 110(2): 213-222. DOI:10.1016/S0092-8674(02)00812-7
|
| [45] |
Tang W, Kim TW, Oses-Prieto JA, et al. BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science, 2008, 321(5888): 557-560. DOI:10.1126/science.1156973
|
| [46] |
Kim TW, Guan S, Sun Y, et al. Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nat Cell Biol, 2009, 11(10): 1254-1260. DOI:10.1038/ncb1970
|
| [47] |
Zhu JY, Li Y, Cao DM, et al. The F-box protein KIB1 mediates brassinosteroid-induced inactivation and degradation of GSK3-like kinases in Arabidopsis. Mol Cell, 2017, 66(5): 648-657. DOI:10.1016/j.molcel.2017.05.012
|
| [48] |
Peng P, Yan ZY, Zhu YY, et al. Regulation of the Arabidopsis GSK3-like kinase brassinosteroid-insensitive 2 through proteasome-mediated protein degradation. Mol Plant, 2008, 1(2): 338-346. DOI:10.1093/mp/ssn001
|
| [49] |
He JX, Gendron JM, Yang Y, et al. The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis. PNAS, 2002, 99(15): 10185-10190. DOI:10.1073/pnas.152342599
|
| [50] |
Jiang JJ, Zhang C, Wang XL. A recently evolved isoform of the transcription factor BES1 promotes brassinosteroid signaling and development in Arabidopsis thaliana. Plant Cell, 2015, 27(2): 361-374. DOI:10.1105/tpc.114.133678
|
| [51] |
Vert G, Chory J. Downstream nuclear events in brassinosteroid signalling. Nature, 2006, 441(7089): 96-100. DOI:10.1038/nature04681
|
| [52] |
Wang X, Chory J. Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science, 2006, 313(5790): 1118-1122. DOI:10.1126/science.1127593
|
| [53] |
Gampala SS, Kim TW, He JX, et al. An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis. Dev Cell, 2007, 13(2): 177-189. DOI:10.1016/j.devcel.2007.06.009
|
| [54] |
Peng J, Richards DE, Hartley NM, et al. 'Green revolution' genes encode mutant gibberellin response modulators. Nature, 1999, 400(6741): 256-261. DOI:10.1038/22307
|
| [55] |
Chandler PM, Harding CA. 'Overgrowth' mutants in barley and wheat: new alleles and phenotypes of the 'green revolution' Della gene. J Exp Bot, 2013, 64(6): 1603-1613. DOI:10.1093/jxb/ert022
|
| [56] |
Derkx AP, Harding CA, Miraghazadeh A, et al. Overgrowth (Della) mutants of wheat: development, growth and yield of intragenic suppressors of the Rht-B1c dwarfing gene. Funct Plant Biol, 2017, 44(5): 525-537. DOI:10.1071/FP16262
|
| [57] |
Nawaz G, Usman B, Zhao N, et al. CRISPR/Cas9 directed mutagenesis of OsGA20ox2 in high yielding basmati rice (Oryza sativa L.) line and comparative proteome profiling of unveiled changes triggered by mutations. Int J Mol Sci, 2020, 21(17): 6170. DOI:10.3390/ijms21176170
|
| [58] |
Li QF, Wang C, Jiang L, et al. An interaction between BZR1 and DELLAs mediates direct signaling crosstalk between brassinosteroids and gibberellins in Arabidopsis. Sci Signal, 2012, 5(244): ra72.
|
| [59] |
Li QF, He JX. Mechanisms of signaling crosstalk between brassinosteroids and gibberellins. Plant Signal Behav, 2013, 8(7): e24686. DOI:10.4161/psb.24686
|
| [60] |
Tong H, Xiao Y, Liu D, et al. Brassinosteroid regulates cell elongation by modulating gibberellin metabolism in rice. Plant Cell, 2014, 26(11): 4376-4393. DOI:10.1105/tpc.114.132092
|
| [61] |
Zhang J, Liu X, Li S, et al. The rice semi-dwarf mutant sd37, caused by a mutation in CYP96B4, plays an important role in the fine-tuning of plant growth. PLoS One, 2014, 9(2): e88068. DOI:10.1371/journal.pone.0088068
|
| [62] |
Tong H, Liu L, Jin Y, et al. Dwarf and low-tillering acts as a direct downstream target of a GSK3/SHAGGY-like kinase to mediate brassinosteroid responses in rice. Plant Cell, 2012, 24(6): 2562-2577. DOI:10.1105/tpc.112.097394
|
| [63] |
Xiao Y, Liu D, Zhang G, et al. Brassinosteroids regulate OFP1, a DLT interacting protein, to modulate plant architecture and grain morphology in rice. Front Plant Sci, 2017, 8: 1698. DOI:10.3389/fpls.2017.01698
|
| [64] |
Gao J, Chen H, Yang HF, et al. A brassinosteroid responsive miRNA-target module regulates gibberellin biosynthesis and plant development. New Phytol, 2018, 220(2): 488-501. DOI:10.1111/nph.15331
|
| [65] |
Tang YY, Liu HH, Guo SY, et al. OsmiR396d affects gibberellin and brassinosteroid signaling to regulate plant architecture in rice. Plant Physiol, 2018, 176(1): 946-959. DOI:10.1104/pp.17.00964
|
| [66] |
Li D, Wang L, Wang M, et al. Engineering OsBAK1 gene as a molecular tool to improve rice architecture for high yield. Plant Biotechnol J, 2009, 7(8): 791-806. DOI:10.1111/j.1467-7652.2009.00444.x
|
| [67] |
Yang ZJ, Yan BQ, Dong HX, et al. BIC1 acts as a transcriptional coactivator to promote brassinosteroid signaling and plant growth. Embo J, 2021, 40(1): e104615.
|
| [68] |
Mantilla-Perez MB, Salas Fernandez MG. Differential manipulation of leaf angle throughout the canopy: current status and prospects. J Exp Bot, 2017, 68(21/22): 5699-5717.
|
| [69] |
Li X, Wu PF, Lu Y, et al. Synergistic interaction of phytohormones in determining leaf angle in crops. Int J Mol Sci, 2020, 21(14): 5052. DOI:10.3390/ijms21145052
|
| [70] |
Sakamoto T, Morinaka Y, Ohnishi T, et al. Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice. Nat Biotechnol, 2006, 24(1): 105-109. DOI:10.1038/nbt1173
|
| [71] |
Hong Z, Ueguchi-Tanaka M, Umemura K, et al. A rice brassinosteroid-deficient mutant, ebisu dwarf (d2), is caused by a loss of function of a new member of cytochrome P450. Plant Cell, 2003, 15(12): 2900-2910. DOI:10.1105/tpc.014712
|
| [72] |
Hong Z, Ueguchi-Tanaka M, Shimizu-Sato S, et al. Loss-of-function of a rice brassinosteroid biosynthetic enzyme, C-6 oxidase, prevents the organized arrangement and polar elongation of cells in the leaves and stem. Plant J, 2002, 32(4): 495-508. DOI:10.1046/j.1365-313X.2002.01438.x
|
| [73] |
Mori M, Nomura T, Ooka H, et al. Isolation and characterization of a rice dwarf mutant with a defect in brassinosteroid biosynthesis. Plant Physiol, 2002, 130(3): 1152-1161. DOI:10.1104/pp.007179
|
| [74] |
Tanabe S, Ashikari M, Fujioka S, et al. A novel cytochrome P450 is implicated in brassinosteroid biosynthesis via the characterization of a rice dwarf mutant, dwarf11, with reduced seed length. Plant Cell, 2005, 17(3): 776-790. DOI:10.1105/tpc.104.024950
|
| [75] |
Yamamuro C, Ihara Y, Wu X, et al. Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell, 2000, 12(9): 1591-1606. DOI:10.1105/tpc.12.9.1591
|
| [76] |
Bai MY, Zhang LY, Gampala SS, et al. Functions of OsBZR1 and 14-3-3 proteins in brassinosteroid signaling in rice. PNAS, 2007, 104(34): 13839-13844. DOI:10.1073/pnas.0706386104
|
| [77] |
Zhang C, Xu Y, Guo S, et al. Dynamics of brassinosteroid response modulated by negative regulator LIC in rice. PLoS Genet, 2012, 8(4): e1002686. DOI:10.1371/journal.pgen.1002686
|
| [78] |
Hirano K, Yoshida H, Aya K, et al. Small organ size 1 and small organ size 2/dwarf and low-tillering form a complex to integrate auxin and brassinosteroid signaling in rice. Mol Plant, 2017, 10(4): 590-604. DOI:10.1016/j.molp.2016.12.013
|
| [79] |
Qiao S, Sun S, Wang L, et al. The RLA1/SMOS1 transcription factor functions with OsBZR1 to regulate brassinosteroid signaling and rice architecture. Plant Cell, 2017, 29(2): 292-309. DOI:10.1105/tpc.16.00611
|
| [80] |
Tanaka A, Nakagawa H, Tomita C, et al. Brassinosteroid upregulated1, encoding a helix-loop-helix protein, is a novel gene involved in brassinosteroid signaling and controls bending of the lamina joint in rice. Plant Physiol, 2009, 151(2): 669-680. DOI:10.1104/pp.109.140806
|
| [81] |
Zhang LY, Bai MY, Wu JX, et al. Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis. Plant Cell, 2010, 21(12): 3767-3780. DOI:10.1105/tpc.109.070441
|
| [82] |
Wang K, Li MQ, Chang YP, et al. The basic helix-loop-helix transcription factor OsBLR1 regulates leaf angle in rice via brassinosteroid signalling. Plant Mol Biol, 2020, 102(6): 589-602. DOI:10.1007/s11103-020-00965-5
|
| [83] |
Seo H, Kim SH, Lee BD, et al. The rice basic helix–loop–helix 79 (OsbHLH079) determines leaf angle and grain shape. Int J Mol Sci, 2020, 21(6): 2090. DOI:10.3390/ijms21062090
|
| [84] |
Tian XJ, Li XF, Zhou WJ, et al. Transcription factor OsWRKY53 positively regulates brassinosteroid signaling and plant architecture. Plant Physiol, 2017, 175(3): 1337-1349. DOI:10.1104/pp.17.00946
|
| [85] |
Li ZC, He YH. Roles of brassinosteroids in plant reproduction. Int J Mol Sci, 2020, 21(3): 872. DOI:10.3390/ijms21030872
|
| [86] |
Gendron JM, Liu JS, Fan M, et al. Brassinosteroids regulate organ boundary formation in the shoot apical meristem of Arabidopsis. PNAS, 2012, 109(51): 21152-21157. DOI:10.1073/pnas.1210799110
|
| [87] |
Bell EM, Lin WC, Husbands AY, et al. Arabidopsis lateral organ boundaries negatively regulates brassinosteroid accumulation to limit growth in organ boundaries. PNAS, 2012, 109(51): 21146-21151. DOI:10.1073/pnas.1210789109
|
| [88] |
Li Y, Li X, Fu D, et al. Panicle morphology mutant 1 (PMM1) determines the inflorescence architecture of rice by controlling brassinosteroid biosynthesis. BMC Plant Biol, 2018, 18(1): 348. DOI:10.1186/s12870-018-1577-x
|
| [89] |
Wu Y, Fu Y, Zhao S, et al. Clustered primary branch 1, a new allele of dwarf11, controls panicle architecture and seed size in rice. Plant Biotechnol J, 2016, 14(1): 377-386. DOI:10.1111/pbi.12391
|
| [90] |
Zhou Y, Tao Y, Zhu J, et al. GNS4, a novel allele of dwarf11, regulates grain number and grain size in a high-yield rice variety. Rice (N Y), 2017, 10(1): 34. DOI:10.1186/s12284-017-0171-4
|
| [91] |
Yuan H, Fan SJ, Huang J, et al. 08SG2/OsBAK1 regulates grain size and number, and functions differently in Indica and Japonica backgrounds in rice. Rice (N Y), 2017, 10(1): 25. DOI:10.1186/s12284-017-0165-2
|
| [92] |
Bai X, Huang Y, Hu Y, et al. Duplication of an upstream silencer of FZP increases grain yield in rice. Nat Plants, 2017, 3(11): 885-893. DOI:10.1038/s41477-017-0042-4
|
| [93] |
Xu H, Liu Q, Yao T, et al. Shedding light on integrative GA signaling. Curr Opin Plant Biol, 2014, 21: 89-95. DOI:10.1016/j.pbi.2014.06.010
|
| [94] |
Yamada Y, Furusawa S, Nagasaka S, et al. Strigolactone signaling regulates rice leaf senescence in response to a phosphate deficiency. Planta, 2014, 240(2): 399-408.
|
| [95] |
Yamaguchi N, Winter CM, Wu MF, et al. Gibberellin acts positively then negatively to control onset of flower formation in Arabidopsis. Science, 2014, 344(6184): 638-641. DOI:10.1126/science.1250498
|
| [96] |
Yu S, Galv o VC, Zhang YC, et al. Gibberellin regulates the Arabidopsis floral transition through miR156-targeted SQUAMOSA promoter binding-like transcription factors. Plant Cell, 2012, 24(8): 3320-3332. DOI:10.1105/tpc.112.101014
|
| [97] |
Serrano-Mislata A, Bencivenga S, Bush M, et al. Della genes restrict inflorescence meristem function independently of plant height. Nat Plants, 2017, 3(9): 749-754. DOI:10.1038/s41477-017-0003-y
|
| [98] |
Tong XH, Wang YF, Sun AQ, et al. Notched belly grain 4, a novel allele of dwarf 11, regulates grain shape and seed germination in rice (Oryza sativa L. Int J Mol Sci, 2018, 19(12): E4069. DOI:10.3390/ijms19124069
|
| [99] |
Lin Y, Zhao Z, Zhou S, et al. Top bending panicle1 is involved in brassinosteroid signaling and regulates the plant architecture in rice. Plant Physiol Biochem, 2017, 121: 1-13. DOI:10.1016/j.plaphy.2017.10.001
|
| [100] |
Liu X, Yang CY, Miao R, et al. DS1/OsEMF1 interacts with OsARF11 to control rice architecture by regulation of brassinosteroid signaling. Rice (N Y), 2018, 11(1): 46. DOI:10.1186/s12284-018-0239-9
|
| [101] |
Qin R, Zeng DD, Yang CC, et al. LTBSG1, a new allele of BRD2, regulates panicle and grain development in rice by brassinosteroid biosynthetic pathway. Genes (Basel), 2018, 9(6): E292. DOI:10.3390/genes9060292
|
| [102] |
Sun F, Ding L, Feng W, et al. Maize transcription factor ZmBES1/BZR1-5 positively regulates kernel size. J Exp Bot, 2021, 72(5): 1714-1726. DOI:10.1093/jxb/eraa544
|
| [103] |
Yang C, Ma Y, He Y, et al. OsOFP19 modulates plant architecture by integrating the cell division pattern and brassinosteroid signaling. Plant J, 2018, 93(3): 489-501. DOI:10.1111/tpj.13793
|
| [104] |
Xiao Y, Zhang G, Liu D, et al. GSK2 stabilizes OFP3 to suppress brassinosteroid responses in rice. Plant J, 2020, 102(6): 1187-1201. DOI:10.1111/tpj.14692
|
| [105] |
Liu J, Shi Y, Yang S. Insights into the regulation of C-repeat binding factors in plant cold signaling. J Integr Plant Biol, 2018, 60(9): 780-795. DOI:10.1111/jipb.12657
|
| [106] |
Yang Y, Guo Y. Unraveling salt stress signaling in plants. J Integr Plant Biol, 2018, 60(9): 796-804. DOI:10.1111/jipb.12689
|
| [107] |
López-Maury L, Marguerat S, B hler J. Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation. Nat Rev Genet, 2008, 9(8): 583-593.
|
| [108] |
Shi Y, Ding Y, Yang S. Molecular regulation of CBF signaling in cold acclimation. Trends Plant Sci, 2018, 23(7): 623-637. DOI:10.1016/j.tplants.2018.04.002
|
| [109] |
Jia Y, Ding Y, Shi Y, et al. The cbfs triple mutants reveal the essential functions of CBFs in cold acclimation and allow the definition of CBF regulons in Arabidopsis. New Phytol, 2016, 212(2): 345-353. DOI:10.1111/nph.14088
|
| [110] |
Zhao C, Zhang Z, Xie S, et al. Mutational evidence for the critical role of CBF transcription factors in cold acclimation in Arabidopsis. Plant Physiol, 2016, 171(4): 2744-2759. DOI:10.1104/pp.16.00533
|
| [111] |
Novillo F, Alonso JM, Ecker JR, et al. CBF2/ DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. PNAS, 2004, 101(11): 3985-3990. DOI:10.1073/pnas.0303029101
|
| [112] |
Zhao C, Wang P, Si T, et al. MAP kinase cascades regulate the cold response by modulating ICE1 protein stability. Dev Cell, 2017, 43(5): 618-629. DOI:10.1016/j.devcel.2017.09.024
|
| [113] |
Chinnusamy V, Ohta M, Kanrar S, et al. ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev, 2003, 17(8): 1043-1054. DOI:10.1101/gad.1077503
|
| [114] |
Doherty CJ, Van Buskirk HA, Myers SJ, et al. Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell, 2009, 21(3): 972-984. DOI:10.1105/tpc.108.063958
|
| [115] |
Kim Y, Park S, Gilmour SJ, et al. Roles of CAMTA transcription factors and salicylic acid in configuring the low-temperature transcriptome and freezing tolerance of Arabidopsis. Plant J, 2013, 75(3): 364-376. DOI:10.1111/tpj.12205
|
| [116] |
Shi Y, Tian S, Hou L, et al. Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis. Plant Cell, 2012, 24(6): 2578-2595. DOI:10.1105/tpc.112.098640
|
| [117] |
Jiang B, Shi Y, Zhang X, et al. PIF3 is a negative regulator of the CBF pathway and freezing tolerance in Arabidopsis. PNAS, 2017, 114(32): E6695-E6702. DOI:10.1073/pnas.1706226114
|
| [118] |
Guo XY, Liu DF, Chong K. Cold signaling in plants: insights into mechanisms and regulation. J Integr Plant Biol, 2018, 60(9): 745-756. DOI:10.1111/jipb.12706
|
| [119] |
Ding Y, Li H, Zhang X, et al. OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Dev Cell, 2015, 32(3): 278-289. DOI:10.1016/j.devcel.2014.12.023
|
| [120] |
Ding YL, Jia YX, Shi YT, et al. OST1-mediated BTF3L phosphorylation positively regulates CBFs during plant cold responses. EMBO J, 2018, 37(8): e98228.
|
| [121] |
Ding YL, Lv J, Shi YT, et al. EGR2 phosphatase regulates OST1 kinase activity and freezing tolerance in Arabidopsis. EMBO J, 2019, 38(1): e99819.
|
| [122] |
Li H, Ding Y, Shi Y, et al. MPK3-and MPK6-mediated ICE1 phosphorylation negatively regulates ICE1 stability and freezing tolerance in Arabidopsis. Dev Cell, 2017, 43(5): 630-642. DOI:10.1016/j.devcel.2017.09.025
|
| [123] |
Zhang Z, Li J, Li F, et al. OsMAPK3 phosphorylates OsbHLH002/OsICE1 and inhibits its ubiquitination to activate OsTPP1 and enhances rice chilling tolerance. Dev Cell, 2017, 43(6): 731-743. DOI:10.1016/j.devcel.2017.11.016
|
| [124] |
Liu ZY, Jia YX, Ding YL, et al. Plasma membrane CRPK1-mediated phosphorylation of 14-3-3 proteins induces their nuclear import to fine-tune CBF signaling during cold response. Mol Cell, 2017, 66(1): 117-128. DOI:10.1016/j.molcel.2017.02.016
|
| [125] |
Ye K, Li H, Ding Y, et al. Brassinosteroid- insensitive2 negatively regulates the stability of transcription factor ICE1 in response to cold stress in Arabidopsis. Plant Cell, 2019, 31(11): 2682-2696.
|
| [126] |
Li H, Ye K, Shi Y, et al. BZR1 positively regulates freezing tolerance via CBF-dependent and CBF-independent pathways in Arabidopsis. Mol Plant, 2017, 10(4): 545-559. DOI:10.1016/j.molp.2017.01.004
|
| [127] |
Li J, Zhou H, Zhang Y, et al. The GSK3-like kinase BIN2 is a molecular switch between the salt stress response and growth recovery in Arabidopsis thaliana. Dev Cell, 2020, 55(3): 367-380. DOI:10.1016/j.devcel.2020.08.005
|
| [128] |
Dal Santo S, Stampfl H, Krasensky J, et al. Stress-induced GSK3 regulates the redox stress response by phosphorylating glucose-6-phosphate dehydrogenase in Arabidopsis. Plant Cell, 2012, 24(8): 3380-3392. DOI:10.1105/tpc.112.101279
|
| [129] |
Xie Z, Nolan T, Jiang H, et al. The AP2/ERF transcription factor TINY modulates brassinosteroid- regulated plant growth and drought responses in Arabidopsis. Plant Cell, 2019, 31(8): 1788-1806. DOI:10.1105/tpc.18.00918
|
| [130] |
Chaves-Sanjuan A, Sanchez-Barrena MJ, Gonzalez-Rubio JM, et al. Structural basis of the regulatory mechanism of the plant CIPK family of protein kinases controlling ion homeostasis and abiotic stress. PNAS, 2014, 111(42): E4532-E4541. DOI:10.1073/pnas.1407610111
|
| [131] |
Nolan TM, Vukašinović N, Liu D, et al. Brassinosteroids: multidimensional regulators of plant growth, development, and stress responses. Plant Cell, 2020, 32(2): 295-318. DOI:10.1105/tpc.19.00335
|
| [132] |
Bai MY, Shang JX, Oh E, et al. Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol, 2012, 14(8): 810-817. DOI:10.1038/ncb2546
|
| [133] |
Cho H, Ryu H, Rho S, et al. A secreted peptide acts on BIN2-mediated phosphorylation of ARFs to potentiate auxin response during lateral root development. Nat Cell Biol, 2014, 16(1): 66-76. DOI:10.1038/ncb2893
|
| [134] |
Wang H, Tang J, Liu J, et al. Abscisic acid signaling inhibits brassinosteroid signaling through dampening the dephosphorylation of BIN2 by ABI1 and ABI2. Mol Plant, 2018, 11(2): 315-325. DOI:10.1016/j.molp.2017.12.013
|
| [135] |
Suzuki T, Bridges D, Nakada D, et al. Inhibition of AMPK catabolic action by GSK3. Mol Cell, 2013, 50(3): 407-419. DOI:10.1016/j.molcel.2013.03.022
|
| [136] |
Ma L, Ye J, Yang Y, et al. The SOS2-SCaBP8 complex generates and fine-tunes an AtANN4-dependent calcium signature under salt stress. Dev Cell, 2019, 48(5): 697-709. DOI:10.1016/j.devcel.2019.02.010
|
| [137] |
Zhang SS, Cai ZY, Wang XL. The primary signaling outputs of brassinosteroids are regulated by abscisic acid signaling. PNAS, 2009, 106(11): 4543-4548. DOI:10.1073/pnas.0900349106
|
| [138] |
Cui F, Liu LJ, Zhao QZ, et al. Arabidopsis ubiquitin conjugase UBC32 is an ERAD component that functions in brassinosteroid-mediated salt stress tolerance. Plant Cell, 2012, 24(1): 233-244. DOI:10.1105/tpc.111.093062
|
| [139] |
Zhao X, Dou L, Gong Z, et al. BES1 hinders abscisic acid insensitive5 and promotes seed germination in Arabidopsis. New Phytol, 2019, 221(2): 908-918. DOI:10.1111/nph.15437
|
| [140] |
Geng Y, Wu R, Wee CW, et al. A spatio-temporal understanding of growth regulation during the salt stress response in Arabidopsis. Plant Cell, 2013, 25(6): 2132-2154. DOI:10.1105/tpc.113.112896
|
| [141] |
Julkowska MM, Testerink C. Tuning plant signaling and growth to survive salt. Trends Plant Sci, 2015, 20(9): 586-594. DOI:10.1016/j.tplants.2015.06.008
|