Progress of research on hormone regulation of branching or tillering in plants

doi:10.11686/cyxb2023118

Abstract

Abstract:

Branching （or tillering in grasses and related taxa） is an important trait of plant architecture and the result of axillary bud initiation and growth， which plays a crucial role in determining the seed yield of crops and forage yield. Multiple hormones and their interactions play key regulatory roles in the occurrence， growth and development of plant branching or tillering. In addition， environmental factors also regulate branching or tillering by changing the hormone contents and their balances within the plant. This study reviews multiple aspects of the mechanisms by which plant branching or tillering is regulated various hormones， including auxin， cytokinin， strigolactones， brassinosteroids， abscisic acid and gibberellins， ethylene， jasmonic acid， and complex regulatory networks formed by the interaction of different hormone signals. The aim is to establish a foundation for using hormone regulation mechanisms to cultivate new high-yielding crop plant growth forms with ideal plant architecture. The current issues with hormone regulation mechanisms controlling plant branching or tillering are also analyzed， and future research directions for hormone regulation mechanisms controlling plant branching or tillering are discussed， with the aim of providing a theoretical basis for using hormones to cultivate good varieties.

Key words: plant hormones, plant architecture, axillary meristem, lateral meristems, branches/tillers

Fen-qi CHEN, Jin-qing ZHANG, Hui-ling MA. Progress of research on hormone regulation of branching or tillering in plants[J]. Acta Prataculturae Sinica, 2024, 33(2): 212-225.

Figures/Tables 3

References 124

1	Hu J， Sun S， Wang X. Regulation of shoot branching by strigolactones and brassinosteroids： conserved and specific functions of Arabidopsis BES1 and rice BZR1. Molecular Plant， 2020， 13（6）： 808-810.
2	Zhao D， Atlin G， Bastiaans L， et al. Developing selection protocols for weed competitiveness in aerobic rice. Field Crops Research， 2006， 97（2/3）： 272-285.
3	Simon S， Morel K， Durand E， et al. Aphids at crossroads： when branch architecture alters aphid infestation patterns in the apple tree. Trees， 2012， 26（1）： 273-282.
4	Doebley J， Gaut B， Smith B. The molecular genetics of crop domestication. Cell， 2006， 127（7）： 1309-1321.
5	Duan E， Wang Y， Li X， et al. OsSHI1 regulates plant architecture through modulating the transcriptional activity of IPA1 in rice. The Plant Cell， 2019， 31（5）： 1026-1042.
6	Bauer B， Von W N. Modulating tiller formation in cereal crops by the signaling function of fertilizer nitrogen forms. Scientific Reports， 2020， 10（1）： 20504.
7	Li L， Xie C， Zong J， et al. Physiological and comparative transcriptome analyses of the high-tillering mutant mtn1 reveal regulatory mechanisms in the tillering of centipede grass ［Eremochloa ophiuroides （Munro） Hack.］. International Journal of Molecular Sciences， 2022， 23（19）： 11580.
8	Gou J， Debnath S， Sun L， et al. From model to crop： functional characterization of SPL8 in M. truncatula led to genetic improvement of biomass yield and abiotic stress tolerance in alfalfa. Plant Biotechnology Journal， 2018， 16（4）： 951-962.
9	Xia Y T， Wang C， Hao N， et al. Research progress on plant branchiness and its application in vegetable breeding. China Vegetables， 2022（1）： 31-40.
	夏雨桐，王琛，郝宁，等. 植物分枝性研究进展及其在蔬菜育种中的应用. 中国蔬菜， 2022（1）： 31-40.
10	Liu T， Wang T H， Chun Y， et al. Research progresses on epigenetic regulation of plant branching/tillering. Chinese Bulletin of Botany， 2022， 57（4）： 532-548.
	刘婷，王天浩，淳雁，等. 表观遗传调控植物分枝/分蘖研究进展. 植物学报， 2022， 57（4）： 532-548.
11	Wang B， Smith S M， Li J. Genetic regulation of shoot architecture. Annual Review of Plant Biology， 2018， 69： 437-468.
12	Ward S P， Leyser O. Shoot branching. Current Opinion in Plant Biology， 2004， 7（1）： 73-78.
13	Guo D， Zhang J， Wang X， et al. The WRKY transcription factor WRKY71/EXB1 controls shoot branching by transcriptionally regulating RAX genes in Arabidopsis. The Plant Cell， 2015， 27（11）： 3112-3127.
14	Lu Z， Yu H， Xiong G， et al. Genome-wide binding analysis of the transcription activator ideal plant architecture 1 reveals a complex network regulating rice plant architecture. The Plant Cell， 2013， 25（10）： 3743-3759.
15	González-Grandío E， Pajoro A， Franco-Zorrilla J M， et al. Abscisic acid signaling is controlled by a BRANCHED1/HD-ZIP I cascade in Arabidopsis axillary buds. Proceedings of the National Academy of Sciences of the United States of America， 2017， 114（2）： E245-E254.
16	Wang M， Le Moigne M A， Bertheloot J， et al. BRANCHED1： a key hub of shoot branching. Frontiers in Plant Science， 2019， 10： 76.
17	Zhang X， Lin Z， Wang J， et al. The tin1 gene retains the function of promoting tillering in maize. Nature Communications， 2019， 10（1）： 5608.
18	Rameau C， Bertheloot J， Leduc N， et al. Multiple pathways regulate shoot branching. Frontiers in Plant Science， 2014， 5： 741.
19	Kariali E， Mohapatra P K. Hormonal regulation of tiller dynamics in differentially-tillering rice cultivars. Plant Growth Regulation， 2007， 53（3）： 215-223.
20	Dun E A， Ferguson B J， Beveridge C A. Apical dominance and shoot branching. Divergent opinions or divergent mechanisms？ Plant Physiology， 2006， 142（3）： 812-819.
21	Seale M， Bennett T， Leyser O. BRC1 expression regulates bud activation potential but is not necessary or sufficient for bud growth inhibition in Arabidopsis. Development， 2017， 144（9）： 1661-1673.
22	Xia X， Dong H， Yin Y， et al. Brassinosteroid signaling integrates multiple pathways to release apical dominance in tomato. Proceedings of the National Academy of Sciences of the United States of America， 2021， 118（11）： e2004384118.
23	Xu J， Zha M， Li Y， et al. The interaction between nitrogen availability and auxin， cytokinin， and strigolactone in the control of shoot branching in rice （Oryza sativa L.）. Plant Cell Reports， 2015， 34（9）： 1647-1662.
24	Blakeslee J J， Bandyopadhyay A， Lee O R， et al. Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. The Plant Cell， 2007， 19（1）： 131-147.
25	Bennett T， Sieberer T， Willett B， et al. The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Current Biology， 2006， 16（6）： 553-563.
26	Wang Q， Kohlen W， Rossmann S， et al. Auxin depletion from the leaf axil conditions competence for axillary meristem formation in Arabidopsis and tomato. The Plant Cell， 2014， 26（5）： 2068-2079.
27	Wang Y， Wang J， Shi B， et al. The stem cell niche in leaf axils is established by auxin and cytokinin in Arabidopsis. The Plant Cell， 2014， 26（5）： 2055-2067.
28	Booker J， Chatfield S， Leyser O. Auxin acts in xylem-associated or medullary cells to mediate apical dominance. The Plant Cell， 2003， 15（2）： 495-507.
29	Waldie T， Mcculloch H， Leyser O. Strigolactones and the control of plant development： lessons from shoot branching. The Plant Journal， 2014， 79（4）： 607-622.
30	Ferguson B J， Beveridge C A. Roles for auxin， cytokinin， and strigolactone in regulating shoot branching. Plant Physiology， 2009， 149（4）： 1929-1944.
31	Ongaro V， Bainbridge K， Williamson L， et al. Interactions between axillary branches of Arabidopsis. Molecular Plant， 2008， 1（2）： 388-400.
32	Xu M， Zhu L， Shou H， et al. A PIN1 family gene， OsPIN1， involved in auxin-dependent adventitious root emergence and tillering in rice. Plant and Cell Physiology， 2005， 46（10）： 1674-1681.
33	Liu W， Yi Z L， Chen Z Y. Research advances in hormone regulation of tillering in rice. Hybrid Rice， 2013， 28（1）： 1-4， 10.
	刘伟，易自力，陈智勇. 水稻分蘖的激素调控研究进展. 杂交水稻， 2013， 28（1）： 1-4， 10.
34	Wu X， Mcsteen P. The role of auxin transport during inflorescence development in maize （Zea mays， Poaceae）. American Journal of Botany， 2007， 94（11）： 1745-1755.
35	Fang Z G， Yang Q， Xie J T， et al. The role and mechanism of cytokinin in phytoremediation of heavy metal contaminated soil. Acta Ecologica Sinica， 2022， 42（8）： 3056-3065.
	方治国，杨青，谢俊婷，等. 重金属污染土壤植物修复中细胞分裂素的作用与机制. 生态学报， 2022， 42（8）： 3056-3065.
36	Zürcher E， Müller B. Cytokinin synthesis， signaling， and function-advances and new insights. International Review of Cell and Molecular Biology， 2016， 324： 1-38.
37	Cai T， Meng X， Liu X， et al. Exogenous hormonal application regulates the occurrence of wheat tillers by changing endogenous hormones. Frontiers in Plant Science， 2018， 9： 1886.
38	Dun E A， De Saint G A， Rameau C， et al. Antagonistic action of strigolactone and cytokinin in bud outgrowth control. Plant Physiology， 2012， 158（1）： 487-498.
39	Müller D， Waldie T， Miyawaki K， et al. Cytokinin is required for escape but not release from auxin mediated apical dominance. The Plant Journal， 2015， 82（5）： 874-886.
40	Tantikanjana T， Yong J W， Letham D S， et al. Control of axillary bud initiation and shoot architecture in Arabidopsis through the SUPERSHOOT gene. Genes and Development， 2001， 15（12）： 1577-1588.
41	Young N F， Ferguson B J， Antoniadi I， et al. Conditional auxin response and differential cytokinin profiles in shoot branching mutants. Plant Physiology， 2014， 165（4）： 1723-1736.
42	Roman H， Girault T， Barbier F， et al. Cytokinins are initial targets of light in the control of bud outgrowth. Plant Physiology， 2016， 172（1）： 489-509.
43	Guo Y， Gan S. AtMYB2 regulates whole plant senescence by inhibiting cytokinin-mediated branching at late stages of development in Arabidopsis. Plant Physiology， 2011， 156（3）： 1612-1619.
44	Tanaka W， Ohmori Y， Ushijima T， et al. Axillary meristem formation in rice requires the WUSCHEL ortholog TILLERS ABSENT1. The Plant Cell， 2015， 27（4）： 1173-1184.
45	Xin W， Wang Z， Liang Y， et al. Dynamic expression reveals a two-step patterning of WUS and CLV3 during axillary shoot meristem formation in Arabidopsis. Journal of Plant Physiology， 2017， 214： 1-6.
46	Wang J， Tian C， Zhang C， et al. Cytokinin signaling activates WUSCHEL expression during axillary meristem initiation. The Plant Cell， 2017， 29（6）： 1373-1387.
47	Wang H， Li X， Wolabu T， et al. WOX family transcriptional regulators modulate cytokinin homeostasis during leaf blade development in Medicago truncatula and Nicotiana sylvestris. The Plant Cell， 2022， 34（10）： 3737-3753.
48	Zhang T Q， Lian H， Zhou C M， et al. A two-step model for de novo activation of WUSCHEL during plant shoot regeneration. The Plant Cell， 2017， 29（5）： 1073-1087.
49	Meng W J， Cheng Z J， Sang Y L， et al. Type-B Arabidopsis response regulators specify the shoot stem cell niche by dual regulation of WUSCHEL. The Plant Cell， 2017， 29（6）： 1357-1372.
50	Zwanenburg B， Pospíšil T， Ćavar Z S. Strigolactones： new plant hormones in action. Planta， 2016， 243（6）： 1311-1326.
51	Gomez-roldan V， Fermas S， Brewer P B， et al. Strigolactone inhibition of shoot branching. Nature， 2008， 455（7210）： 189-194.
52	Umehara M， Hanada A， Yoshida S， et al. Inhibition of shoot branching by new terpenoid plant hormones. Nature， 2008， 455（7210）： 195-200.
53	Chabikwa T G， Brewer P B， Beveridge C A. Initial bud outgrowth occurs independent of auxin flow from out of buds. Plant Physiology， 2019， 179（1）： 55-65.
54	Braun N， De Saint G A， Pillot J P， et al. The pea TCP transcription factor PsBRC1 acts downstream of strigolactones to control shoot branching. Plant Physiology， 2012， 158（1）： 225-238.
55	Arite T， Iwata H， Ohshima K， et al. DWARF10， an RMS1/MAX4/DAD1 ortholog， controls lateral bud outgrowth in rice. The Plant Journal， 2007， 51（6）： 1019-1029.
56	Al-babili S， Bouwmeester H J. Strigolactones， a novel carotenoid-derived plant hormone. Annual Review of Plant Biology， 2015， 66： 161-186.
57	Waters M T， Gutjahr C， Bennett T， et al. Strigolactone signaling and evolution. Annual Review of Plant Biology， 2017， 68： 291-322.
58	Minakuchi K， Kameoka H， Yasuno N， et al. FINE CULM1 （FC1） works downstream of strigolactones to inhibit the outgrowth of axillary buds in rice. Plant and Cell Physiology， 2010， 51（7）： 1127-1135.
59	Chevalier F， Nieminen K， Sánchez-ferrero J C， et al. Strigolactone promotes degradation of DWARF14， an α/β hydrolase essential for strigolactone signaling in Arabidopsis. The Plant Cell， 2014， 26（3）： 1134-1150.
60	Fang Z， Ji Y， Hu J， et al. Strigolactones and brassinosteroids antagonistically regulate the stability of the D53-OsBZR1 complex to determine FC1 expression in rice tillering. Molecular Plant， 2020， 13（4）： 586-597.
61	Hu J， Ji Y， Hu X， et al. BES1 functions as the co-regulator of D53-like SMXLs to inhibit BRC1 expression in strigolactone-regulated shoot branching in Arabidopsis. Plant Communications， 2020， 1（3）： 100014.
62	Machin D C， Hamon-josse M， Bennett T. Fellowship of the rings： a saga of strigolactones and other small signals. The New Phytologist， 2020， 225（2）： 621-636.
63	Yao R， Ming Z， Yan L， et al. DWARF14 is a non-canonical hormone receptor for strigolactone. Nature， 2016， 536（7617）： 469-473.
64	Wang L， Wang B， Jiang L， et al. Strigolactone signaling in Arabidopsis regulates shoot development by targeting D53-Like SMXL repressor proteins for ubiquitination and degradation. The Plant Cell， 2015， 27（11）： 3128-3142.
65	Zhao B， Wu T T， Ma S S， et al. TaD27-B gene controls the tiller number in hexaploid wheat. Plant Biotechnology Journal， 2020， 18（2）： 513-525.
66	Wang L， Wang B， Yu H， et al. Transcriptional regulation of strigolactone signalling in Arabidopsis. Nature， 2020， 583（7815）： 277-281.
67	Soundappan I， Bennett T， Morffy N， et al. SMAX1-LIKE/D53 family members enable distinct MAX2-dependent responses to strigolactones and karrikins in Arabidopsis. The Plant Cell， 2015， 27（11）： 3143-3159.
68	Liang Y， Ward S， Li P， et al. SMAX1-LIKE7 signals from the nucleus to regulate shoot development in Arabidopsis via partially ear motif-independent mechanisms. The Plant Cell， 2016， 28（7）： 1581-1601.
69	Xu J， Ding C， Ding Y. A proteomic approach to analyze differential regulation of proteins during bud outgrowth under apical dominance based on the auxin transport canalization model in rice （Oryza sativa L.）. Journal of Plant Growth Regulation， 2015， 34（1）： 122-136.
70	Dun E A， De Saint G A， Rameau C， et al. Dynamics of strigolactone function and shoot branching responses in Pisum sativum. Molecular Plant， 2013， 6（1）： 128-140.
71	De Saint G A， Ligerot Y， Dun E A， et al. Strigolactones stimulate internode elongation independently of gibberellins. Plant Physiology， 2013， 163（2）： 1012-1025.
72	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.
73	Kapulnik Y， Resnick N， Mayzlish-Gati E， et al. Strigolactones interact with ethylene and auxin in regulating root-hair elongation in Arabidopsis. Journal of Experimental Botany， 2011， 62（8）： 2915-2924.
74	Rasmussen A， Mason M G， De Cuyper C， et al. Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiology， 2012， 158（4）： 1976-1987.
75	Rasmussen A， Heugebaert T， Matthys C， et al. A fluorescent alternative to the synthetic strigolactone GR24. Molecular Plant， 2013， 6（1）： 100-112.
76	Agusti J， Herold S， Schwarz M， et al. Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proceedings of the National Academy of Sciences of the United States of America， 2011， 108（50）： 20242-20247.
77	Wang Y， Shang L， Yu H， et al. A strigolactone biosynthesis gene contributed to the green revolution in rice. Molecular Plant， 2020， 13（6）： 923-932.
78	Lu Z， Shao G， Xiong J， et al. MONOCULM 3， an ortholog of WUSCHEL in rice， is required for tiller bud formation. Journal of Genetics and Genomics， 2015， 42（2）： 71-78.
79	Mjomba F M， Zheng Y， Liu H， et al. Homeobox is pivotal for OsWUS controlling tiller development and female fertility in rice. G3 （Bethesda）， 2016， 6（7）： 2013-2021.
80	Jiang L， Liu X， Xiong G， et al. DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature， 2013， 504（7480）： 401-405.
81	Zhou F， Lin Q， Zhu L， et al. D14-SCF（D3）-dependent degradation of D53 regulates strigolactone signalling. Nature， 2013， 504（7480）： 406-410.
82	Sharma I， Ching E， Saini S， et al. Exogenous application of brassinosteroid offers tolerance to salinity by altering stress responses in rice variety Pusa Basmati-1. Plant Physiology and Biochemistry， 2013， 69： 17-26.
83	Yin Y， Wang Z Y， Mora-Garcia S， et al. BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell， 2002， 109（2）： 181-191.
84	Yin Y， Vafeados D， Tao Y， et al. A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell， 2005， 120（2）： 249-259.
85	Wang Y， Sun S， Zhu W， et al. Strigolactone/MAX2-induced degradation of brassinosteroid transcriptional effector BES1 regulates shoot branching. Developmental Cell， 2013， 27（6）： 681-688.
86	Guo W， Chen L， Herrera-Estrella L， et al. Altering plant architecture to improve performance and resistance. Trends in Plant Science， 2020， 25（11）： 1154-1170.
87	Yao C， Finlayson S A. Abscisic acid is a general negative regulator of Arabidopsis axillary bud growth. Plant Physiology， 2015， 169（1）： 611-626.
88	Liu X， Hu Q， Yan J， et al. ζ-carotene isomerase suppresses tillering in rice through the coordinated biosynthesis of strigolactone and abscisic acid. Molecular Plant， 2020， 13（12）： 1784-1801.
89	Zhan J， Chu Y， Wang Y， et al. The miR164-GhCUC2-GhBRC1 module regulates plant architecture through abscisic acid in cotton. Plant Biotechnology Journal， 2021， 19（9）： 1839-1851.
90	Cline M G， Oh C. A reappraisal of the role of abscisic acid and its interaction with auxin in apical dominance. Annals of Botany， 2006， 98（4）： 891-897.
91	Chatfield S P， Stirnberg P， Forde B G， et al. The hormonal regulation of axillary bud growth in Arabidopsis. The Plant Journal， 2000， 24（2）： 159-169.
92	Liu Y， Ding Y F， Wang Q S， et al. Effect of hormones on the growth of rice tiller bud and the expression of the genes related to tiller growth. Plant Physiology Journal， 2011， 47（4）： 367-372.
	刘杨，丁艳锋，王强盛，等. 激素对水稻分蘖芽生长和分蘖相关基因表达的调控效应. 植物生理学报， 2011， 47（4）： 367-372.
93	Foo E， Bullier E， Goussot M， et al. The branching gene RAMOSUS1 mediates interactions among two novel signals and auxin in pea. The Plant Cell， 2005， 17（2）： 464-474.
94	Confraria A， Muñoz-Gasca A， Ferreira L， et al. Shoot branching phenotyping in Arabidopsis and tomato. Methods in Molecular Biology， 2022， 2494： 47-59.
95	Dong C， Zhang L， Zhang Q， et al. Tiller number 1 encodes an ankyrin repeat protein that controls tillering in bread wheat. Nature Communications， 2023， 14（1）： 836.
96	Lo S F， Yang S Y， Chen K T， et al. A novel class of gibberellin 2-oxidases control semidwarfism， tillering， and root development in rice. The Plant Cell， 2008， 20（10）： 2603-2618.
97	Zhang Q Q， Wang J G， Wang L Y， et al. Gibberellin repression of axillary bud formation in Arabidopsis by modulation of DELLA-SPL9 complex activity. Journal of Integrative Plant Biology， 2020， 62（4）： 421-432.
98	Davière J M， Achard P. Gibberellin signaling in plants. Development， 2013， 140（6）： 1147-1151.
99	Ni J， Gao C， Chen M S， et al. Gibberellin promotes shoot branching in the perennial woody plant Jatropha curcas. Plant and Cell Physiology， 2015， 56（8）： 1655-1666.
100	Lin Q， Zhang Z， Wu F， et al. The APC/C（TE） E3 ubiquitin ligase complex mediates the antagonistic regulation of root growth and tillering by ABA and GA. The Plant Cell， 2020， 32（6）： 1973-1987.
101	Liao Z， Yu H， Duan J， et al. SLR1 inhibits MOC1 degradation to coordinate tiller number and plant height in rice. Nature Communications， 2019， 10（1）： 2738.
102	Cai T， Xu H C， Yin Y P， et al. Mechanisms of tiller occurrence affected by exogenous IAA， GA₃， and ABA in wheat with different spike-types. Acta Agronomica Sinica， 2013， 39（10）： 1835-1842.
	蔡铁，徐海成，尹燕枰，等. 外源IAA、GA₃和ABA影响不同穗型小麦分蘖发生的机制. 作物学报， 2013， 39（10）： 1835-1842.
103	Zhou Y F， Yan T， Zhang J， et al. Effects of exogenous IAA application on endogenous hormone contents and tillering in sorghum. Chinese Journal of Ecology， 2017， 36（8）： 2191-2197.
	周宇飞，闫彤，张姣，等. 外源IAA对高粱幼苗内源激素含量及分蘖发生的影响. 生态学杂志， 2017， 36（8）： 2191-2197.
104	Zhang W D， Zhao L F， Gao Q R， et al. Study on ethylene regulation pathways in the development of young spike branching in wheat// The crop science society of China： 2012 academic annual meeting of the Chinese crop society. Nanchang： The Crop Science Society of China， 2012： 1.
	张卫东，赵兰飞，高庆荣，等. 小麦幼穗分枝发育中乙烯调控途径研究// 中国作物学会： 2012年中国作物学会学术年会论文摘要集.南昌：中国作物学会， 2012： 1.
105	Cao Y. Effects of interaction between jasmonic acid and endophytic fungi on wild barley under salt stress. Lanzhou： Lanzhou University， 2018.
	曹莹. 盐胁迫下茉莉酸与内生真菌互作对野大麦的影响. 兰州：兰州大学， 2018.
106	Shen J， Zhang Y， Ge D， et al. CsBRC1 inhibits axillary bud outgrowth by directly repressing the auxin efflux carrier CsPIN3 in cucumber. Proceedings of the National Academy of Sciences of the United States of America， 2019， 116（34）： 17105-17114.
107	Waldie T， Leyser O. Cytokinin targets auxin transport to promote shoot branching. Plant Physiology， 2018， 177（2）： 803-818.
108	Barbier F， Dun E， Kerr S， et al. An update on the signals controlling shoot branching. Trends in Plant Science， 2019， 24（3）： 220-236.
109	Van R， Bennett T， Ticchiarelli F， et al. Connective auxin transport contributes to strigolactone-mediated shoot branching control independent of the transcription factor BRC1. PLoS Genetics， 2019， 15（3）： e1008023.
110	Domagalska M， Leyser O. Signal integration in the control of shoot branching. Nature Reviews Molecular Cell Biology， 2011， 12（4）： 211-221.
111	Saeed W， Naseem S， Ali Z. Strigolactones biosynthesis and their role in abiotic stress resilience in plants： A critical review. Frontiers in Plant Science， 2017， 8： 1487.
112	Waters M T， Brewer P B， Bussell J D， et al. The Arabidopsis ortholog of rice DWARF27 acts upstream of MAX1 in the control of plant development by strigolactones. Plant Physiology， 2012， 159（3）： 1073-1085.
113	Shinohara N， Taylor C， Leyser O. Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biology， 2013， 11（1）： e1001474.
114	Ligerot Y， De Saint G A， Waldie T， et al. The pea branching RMS2 gene encodes the PsAFB4/5 auxin receptor and is involved in an auxin-strigolactone regulation loop. PLoS Genetics， 2017， 13（12）： e1007089.
115	Brewer P B， Dun E A， Ferguson B J， et al. Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiology， 2009， 150（1）： 482-493.
116	Crawford S， Shinohara N， Sieberer T， et al. Strigolactones enhance competition between shoot branches by dampening auxin transport. Development， 2010， 137（17）： 2905-2913.
117	Prusinkiewicz P， Crawford S， Smith R S， et al. Control of bud activation by an auxin transport switch. Proceedings of the National Academy of Sciences of the United States of America， 2009， 106（41）： 17431-17436.
118	Liang J， Zhao L， Challis R， et al. Strigolactone regulation of shoot branching in chrysanthemum （Dendranthema grandiflorum）. Journal of Experimental Botany， 2010， 61（11）： 3069-3078.
119	Mason M G， Ross J J， Babst B A， et al. Sugar demand， not auxin， is the initial regulator of apical dominance. Proceedings of the National Academy of Sciences of the United States of America， 2014， 111（16）： 6092-6097.
120	Duan J， Yu H， Yuan K， et al. Strigolactone promotes cytokinin degradation through transcriptional activation of CYTOKININ OXIDASE/DEHYDROGENASE 9 in rice. Proceedings of the National Academy of Sciences of the United States of America， 2019， 116（28）： 14319-14324.
121	Bennett T， Hines G， Van Rongen M， et al. Connective auxin transport in the shoot facilitates communication between shoot apices. PLoS Biology， 2016， 14（4）： e1002446.
122	Brewer P B， Dun E A， Gui R， et al. Strigolactone inhibition of branching independent of polar auxin transport. Plant Physiology， 2015， 168（4）： 1820-1829.
123	Song X， Lu Z， Yu H， et al. IPA1 functions as a downstream transcription factor repressed by D53 in strigolactone signaling in rice. Cell Research， 2017， 27（9）： 1128-1141.
124	Wu K， Wang S， Song W， et al. Enhanced sustainable green revolution yield via nitrogen-responsive chromatin modulation in rice. Science， 2020， 367（6478）： eaaz2046.

激素类型 Hormone type	基因 Gene	功能描述 Function description	调控方式 Regulatory method	参考文献 Reference
生长素Indole-3-acetic acid， IAA	PIN3、PIN4、PIN7	IAA输出载体IAA output carrier	负调控Negative regulation	［32］
	ABCB/PGP	IAA输出载体IAA output carrier	负调控Negative regulation	［25］
	AUX/LAX	IAA输入协同转运因子IAA input co-transporter	正调控Positive regulation	［25］
	DII	IAA信号转导相关基因IAA signal transduction related gene	正调控Positive regulation	［10］
	DR5	IAA信号转导基因IAA signal transduction gene	负调控Negative regulation	［10］
	YUC	IAA合成基因IAA synthesis gene	负调控Negative regulation	［33］
细胞分裂素Cytokinin， CK	IPT	CK合成酶关键基因Key genes of CK synthase	正调控Positive regulation	［43］
	ARRs	CK下游的转录激活因子Transcription downstream activating factor of CK	正调控Positive regulation	［46］
	OsCKX9	CK降解基因CK degradation gene	负调控Negative regulation	［120］
独脚金内酯Strigolactone， SL	RMS、MAX、HTD1	SLs合成基因SLs synthesis gene	负调控Negative regulation	［53-55］
	D3、D10、D17、D27、 CCD7、CCD8	SLs合成相关基因SLs synthesis related gene	负调控Negative regulation	［50，64-65，77］
	D53、D14	SLs信号转导相关基因SLs signal transduction related gene	正调控Positive regulation	［68］
油菜素甾醇Brassinosterol， BR	BES1、BZR1、 BEH2、BEH3	BR信号通路正调节因子 BR signaling pathway positive regulatory factor	正调控Positive regulation	［60，83］
脱落酸Abscisic acid， ABA	NCED3	ABA合成基因ABA synthesis gene	负调控Negative regulation	［15］
	TaPYL	ABA受体ABA receptor	负调控Negative regulation	［95］
	TaPP2C	ABA信号转导蛋白ABA signal transduction protein	负调控Negative regulation	［95］

激素类型 Hormone type	基因 Gene	功能描述 Function description	调控方式 Regulatory method	参考文献 Reference
生长素Indole-3-acetic acid， IAA	PIN3、PIN4、PIN7	IAA输出载体IAA output carrier	负调控Negative regulation	［32］
	ABCB/PGP	IAA输出载体IAA output carrier	负调控Negative regulation	［25］
	AUX/LAX	IAA输入协同转运因子IAA input co-transporter	正调控Positive regulation	［25］
	DII	IAA信号转导相关基因IAA signal transduction related gene	正调控Positive regulation	［10］
	DR5	IAA信号转导基因IAA signal transduction gene	负调控Negative regulation	［10］
	YUC	IAA合成基因IAA synthesis gene	负调控Negative regulation	［33］
细胞分裂素Cytokinin， CK	IPT	CK合成酶关键基因Key genes of CK synthase	正调控Positive regulation	［43］
	ARRs	CK下游的转录激活因子Transcription downstream activating factor of CK	正调控Positive regulation	［46］
	OsCKX9	CK降解基因CK degradation gene	负调控Negative regulation	［120］
独脚金内酯Strigolactone， SL	RMS、MAX、HTD1	SLs合成基因SLs synthesis gene	负调控Negative regulation	［53-55］
	D3、D10、D17、D27、 CCD7、CCD8	SLs合成相关基因SLs synthesis related gene	负调控Negative regulation	［50，64-65，77］
	D53、D14	SLs信号转导相关基因SLs signal transduction related gene	正调控Positive regulation	［68］
油菜素甾醇Brassinosterol， BR	BES1、BZR1、 BEH2、BEH3	BR信号通路正调节因子 BR signaling pathway positive regulatory factor	正调控Positive regulation	［60，83］
脱落酸Abscisic acid， ABA	NCED3	ABA合成基因ABA synthesis gene	负调控Negative regulation	［15］
	TaPYL	ABA受体ABA receptor	负调控Negative regulation	［95］
	TaPP2C	ABA信号转导蛋白ABA signal transduction protein	负调控Negative regulation	［95］

[1]	Xiao-ting LIU, Tuo YAO. Screening， identification and characteristics of low-temperature-tolerant plant growth promoting rhizobacteria in alpine meadow [J]. Acta Prataculturae Sinica, 2022, 31(8): 178-187.
[2]	Jia-lin LI, Sheng-lin JIANG, Yun-xia LI, Xiao-yan QUAN, Wen-bo WANG, Qiu-li SHAN, Chun-juan XIE, Ning YIN, Yu-xiang QIN, Li-hua ZHANG, Hong-mei LI, Wen-xing HE. Research progress on regulation mechanism of rhizome development in herbaceous plants of the Poaceae [J]. Acta Prataculturae Sinica, 2022, 31(8): 211-220.
[3]	Zhi-min YANG, Rui XING, Yun-jia DING, Li-li ZHUANG. Analysis of differentially expressed genes in relation to tiller development and plant height based on transcriptomic sequencing of two tall fescue cultivars [J]. Acta Prataculturae Sinica, 2022, 31(1): 145-163.
[4]	ZHANG Yu-tong, SHI Feng-ling. Research progress on plant architecture formation and forage grass plant architecture [J]. Acta Prataculturae Sinica, 2020, 29(9): 203-214.
[5]	ZHAO Xiao-qiang, LU Yan-tian, BAI Ming-xing, XU Ming-xia, PENG Yun-ling, DING Yong-fu, ZHUANG Ze-long, CHEN Fen-qi, ZHANG Da-zhi. Response of maize genotypes with different plant architecture to drought stress [J]. Acta Prataculturae Sinica, 2020, 29(2): 149-162.