The Strigolactones Inhibitory Factor D53/SMXLs: A Review

doi:10.11923/j.issn.2095-4050.cjas2022-0070

Abstract

Abstract:

Strigolactones (SLs) is a new type of plant hormone, which is involved in regulating plant branching, reproductive development, leaf senescence and other biological processes. D53/SMXLs is an inhibitor of monolactone signal transduction pathway, and plays an important role in monolactone signal transduction. The previous studies about strigolactones inhibitory factor D53/SMXLs at home and abroad were reviewed. The discovery, structure, signal transduction mechanism, molecular biological functions and other functions of D53/SMXLs were summarized. At last, it was pointed out that the three aspects of strigolactones signal transduction pathway should be further improved and studied.

Key words: strigolactones, D53/SMXLs, signal transduction, branching development, biological function

WANG Xueling, WANG Ruyue, LI Jihong, WANG Jinnan, WANG Dongyue, NIU Muge, SUN Maotong. The Strigolactones Inhibitory Factor D53/SMXLs: A Review[J]. Journal of Agriculture, 2023, 13(10): 37-43.

Figures/Tables 2

References 62

[1]	SANTNER A, ESTELLE M. Recent advances and emerging trends in plant hormone signalling[J]. Nature, 2009, 459(7250):1071-1078. doi: 10.1038/nature08122
[2]	ALDER A, JAMIL M, MARZORATI M, et al. The path from β-carotene to carlactone, a strigolactone-like plant hormone[J]. Science, 2012, 335(6074):1348-1351. doi: 10.1126/science.1218094 URL
[3]	COOK CE, WHICHARD LP, TURNER B, et al. Germination of witchweed (Striga lutea Lour.): isolation and properties of a potent stimulant[J]. Science (new york, n.y.), 1966, 154(3753):189-1190.
[4]	AKIYAMA K, MATSUZAKI K, HAYASHI H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi[J]. Nature, 2005, 435(7043):824-827. doi: 10.1038/nature03608
[5]	UMEHARA M, HANADA A, YOSHIDA S, et al. Inhibition of shoot branching by new terpenoid plant hormones[J]. Nature, 2008, 455(7210):195-200. doi: 10.1038/nature07272
[6]	黎家, 李传友. 新中国成立70年来植物激素研究进展[J]. 中国科学:生命科学, 2019, 49(10):1227-1281.
[7]	JIANG L, LIU X, XIONG G, et al. DWARF 53 acts as a repressor of strigolactone signalling in rice[J]. Nature, 2013, 504(7480):401-405. doi: 10.1038/nature12870
[8]	ZHOU F, LIN Q, ZHU L, et al. D14-SCF(D3)-dependent degradation of D53 regulates strigolactone signalling[J]. Nature, 2013, 504(7480):406-410. doi: 10.1038/nature12878
[9]	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[J]. Plant cell, 2015, 27(11):3128-3142. doi: 10.1105/tpc.15.00605 URL
[10]	WANG B, WANG Y, LI J. Strigolactones. In: Li JY, Li CY, Smith SM, eds. Hormone metabolism and signaling in plants[J]. London: Academic Press, 2017:327-359.
[11]	KOHLEN W, CHARNIKHOVA T, LIU Q, et al. Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis[J]. Plant physiol, 2011, 155(2):974-987. doi: 10.1104/pp.110.164640 pmid: 21119045
[12]	MAYZLISH-GATI E, DE-CUVPER C, GOORMACHTIG S, et al. Strigolactones are involved in root response to low phosphate conditions in Arabidopsis[J]. Plant physiol, 2012, 160(3):1329-1341.
[13]	ARITE T, UMEHARA M, ISHIKAWA S, et al. d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers[J]. Plant cell physiol, 2009, 50(8):1416-1424. doi: 10.1093/pcp/pcp091 pmid: 19542179
[14]	HAMIAUX C, DRUMMOND R S, JANSSEN B J, et al. DAD2 is an α/β hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone[J]. Current biology, 2012, 22(21):2032-2036. doi: 10.1016/j.cub.2012.08.007 pmid: 22959345
[15]	YAO R, WANG L, LI Y, et al. Rice DWARF14 acts as an unconventional hormone receptor for strigolactone[J]. Journal of experimental botany, 2018, 69(9):2355-2365. doi: 10.1093/jxb/ery014 pmid: 29365172
[16]	YAO R, MING Z, YAN L, et al. DWARF14 is a non-canonical hormone receptor for strigolactone[J]. Nature, 2016, 536(7617):469-473. doi: 10.1038/nature19073
[17]	YAO R, WANG F, MING Z, et al. ShHTL7 is a non-canonical receptor for strigolactones in root parasitic weeds[J]. Cell research, 2017, 27(6):838-841. doi: 10.1038/cr.2017.3 pmid: 28059066
[18]	MARCO B, JOANNE C. The many models of strigolactone signaling[J]. Trends in plant science, 2020, 25:395-400. doi: S1360-1385(19)30334-6 pmid: 31948791
[19]	LIN Q, WANG D, DONG H, et al. Rice APC/C(TE) controls tillering by mediating the degradation of MONOCULM 1[J]. Nature communications, 2012, 3:752. doi: 10.1038/ncomms1716 pmid: 22434195
[20]	XU C, WANG Y, YU Y, et al. Degradation of MONOCULM 1 by APC/C(TAD1) regulates rice tillering[J]. Nature communications, 2012, 3:750. doi: 10.1038/ncomms1743 pmid: 22434193
[21]	LIU Y, WU G, ZHAO Y, et al. DWARF53 interacts with transcription factors UB2/UB3/TSH4 to regulate maize tillering and tassel branching[J]. Plant physiology, 2021, 187(2):947-962. doi: 10.1093/plphys/kiab259 pmid: 34608948
[22]	KATYAYINI N U, RINNE P, VAN DER SCHOOT C. Strigolactone-based node-to-bud signaling may restrain shoot branching in hybrid aspen[J]. Plant cell physiology, 2019, 60(12):2797-2811. doi: 10.1093/pcp/pcz170 URL
[23]	KERR S C, PATIL S B, DE SAINT GERMAIN A, et al. Integration of the SMXL/D53 strigolactone signalling repressors in the model of shoot branching regulation in Pisum sativum[J]. Plant journal, 2021, 107(6):1756-1770. doi: 10.1111/tpj.v107.6 URL
[24]	HANSON P I, WHITEHEART S W. AAA+ proteins: have engine, will work[J]. Nature reviews molecular cell biology, 2005, 6(7):519-529. doi: 10.1038/nrm1684 pmid: 16072036
[25]	NEUWALD A F, ARAVIND L, SPOUGE J L, et al. AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes[J]. Genome research, 1999, 9(1):27-43. pmid: 9927482
[26]	MATIAS P M, BAEK S H, BANDEIRAS T M, et al. The AAA+ proteins Pontin and Reptin enter adult age: from understanding their basic biology to the identification of selective inhibitors[J]. Frontiers in molecular biosciences, 2015, 2:17. doi: 10.3389/fmolb.2015.00017 pmid: 25988184
[27]	MA H, DUAN J, KE J, et al. A D53 repression motif induces oligomerization of TOPLESS corepressors and promotes assembly of a corepressor-nucleosome complex[J]. Science advances, 2017, 3(6):e1601217. doi: 10.1126/sciadv.1601217 URL
[28]	BRAUN N, DE SAINT GERMAIN A, PILLOT J P, et al. The pea TCP transcription factor PsBRC1 acts downstream of Strigolactones to control shoot branching[J]. Plant physiology, 2012, 158(1):225-238. doi: 10.1104/pp.111.182725 pmid: 22045922
[29]	SOUNDAPPAN I, BENNETT T, MORFFY N, et al. SMAX1-LIKE/D53 family members enable distinct MAX2-dependent responses to strigolactones and karrikins in arabidopsis[J]. Plant cell, 2015, 27(11):3143-3159. doi: 10.1105/tpc.15.00562 URL
[30]	国浩平. 杨树PagD53基因的克隆表达及其与PagD14基因的相互作用的研究[D]. 泰安: 山东农业大学, 2020.
[31]	DUAN J, YU H, YUAN K, et al. Strigolactone promotes cytokinin degradation through transcriptional activation of CYTOKININ OXIDASE/DEHYDROGENASE 9 in rice[J]. Proceedings of the national academy of sciences, 2019, 116(28):14319-14324. doi: 10.1073/pnas.1810980116 URL
[32]	姚瑞枫, 谢道昕. 独脚金内酯信号途径的新发现——抑制子也是转录因子[J]. 植物学报, 2020, 55(4):397-402. doi: 10.11983/CBB20099
[33]	WANG L, WANG B, YU H, et al. Transcriptional regulation of strigolactone signalling in Arabidopsis[J]. Nature, 2020, 583(7815):277-281. doi: 10.1038/s41586-020-2382-x
[34]	BEVERIDGE C A. Long-distance signalling and a mutational analysis of branching in pea[J]. Plant growth regulation, 2000, 32(2-3):193-203. doi: 10.1023/A:1010718020095 URL
[35]	BEVERIDGE C A, DUN E A, RAMEAU C. Pea has its tendrils in branching discoveries spanning a century from auxin to strigolactones[J]. Plant physiology, 2009, 151(3):985-990. doi: 10.1104/pp.109.143909 pmid: 19767387
[36]	DUN E A, HANAN J, BEVERIDGE C A. Computational modeling and molecular physiology experiments reveal new insights into shoot branching in pea[J]. Plant cell, 2009b, 21(11):3459-3472. doi: 10.1105/tpc.109.069013 URL
[37]	LIGEROT Y, DE SAINT GERMAIN 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[J]. PloS genetics, 2017, 13(12):e1007089. doi: 10.1371/journal.pgen.1007089 URL
[38]	LINCOLN C, BRITTON J H, ESTELLE M. Growth and development of the axr1 mutants of Arabidopsis[J]. Plant cell, 1990, 2(11):1071-1080. doi: 10.1105/tpc.2.11.1071 pmid: 1983791
[39]	DUN E A, BREWER PB, BEVERIDGE C A. Strigolactones: discovery of the elusive shoot branching hormone[J]. Trends in plant science, 2009, 14(7):364-372. doi: 10.1016/j.tplants.2009.04.003 pmid: 19540149
[40]	SONG X, LU Z, YU H, et al. IPA1 functions as a downstream transcription factor repressed by D53 in strigolactone signaling in rice[J]. Cell research, 2017, 27(9):1128-1141. doi: 10.1038/cr.2017.102 pmid: 28809396
[41]	马洪磊. 植物辅抑制因子TPL/TPR蛋白结构与EAR基序相互作用分子机理研究[D]. 上海: 中国科学院上海药物研究所, 2016.
[42]	WANG L, ZHANG Q. Boosting rice yield by fine-tuning SPL gene expression[J]. Trends in plant science, 2017, 22(8):643-646. doi: S1360-1385(17)30116-4 pmid: 28647102
[43]	LU Z, YU H, XIONG G, et al. Genome-wide binding analysis of the transcription activator ideal plant architecture1 reveals a complex network regulating rice plant architecture[J]. Plant cell, 2013, 25(10):3743-3759. doi: 10.1105/tpc.113.113639 URL
[44]	KERR S C, BEVERIDGE C A. IPA1: a direct target of SL signaling[J]. Cell research, 2017, 27(10):1191-1192. doi: 10.1038/cr.2017.114 pmid: 28884742
[45]	TAKEDA T, SUWA Y, SUZUKI M, et al. The OsTB1 gene negatively regulates lateral branching in rice[J]. Plant journal, 2003, 33(3):513-520. doi: 10.1046/j.1365-313x.2003.01648.x pmid: 12581309
[46]	XIE Y, LIU Y, MA M, et al. Arabidopsis FHY3 and FAR1 integrate light and strigolactone signaling to regulate branching[J]. Nature communications, 2020, 11(1):1955. doi: 10.1038/s41467-020-15893-7 pmid: 32327664
[47]	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[J]. Molecular plant, 2020, 13(4):586-597. doi: S1674-2052(19)30401-0 pmid: 31837469
[48]	LI J, NAM K H. Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase[J]. Science, 2002, 295(5558):1299-1301. doi: 10.1126/science.1065769 pmid: 11847343
[49]	LIU J, CHENG X, LIU P, et al. miR156-Targeted SBP-Box transcription factors interact with DWARF53 to regulate TEOSINTE BRANCHED1 and BARREN STALK1 expression in bread wheat[J]. Plant physiology, 2017, 174(3):1931-1948. doi: 10.1104/pp.17.00445 URL
[50]	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[J]. Plant communications, 2019, 1(3):100014. doi: 10.1016/j.xplc.2019.100014 URL
[51]	DOEBLEY J, STEC A, GUSTUS C. Teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance[J]. Genetics, 1995, 141(1):333-346. doi: 10.1093/genetics/141.1.333 pmid: 8536981
[52]	MASON M G, ROSS J J, BABST B A, et al. Sugar demand, not auxin, is the initial regulator of apical dominance[J]. Proceedings of the national academy of sciences, 2014, 111(16):6092-6097. doi: 10.1073/pnas.1322045111 URL
[53]	QU B, QIN Y, BAI Y. From signaling to function: how strigolactones regulate plant development[J]. Science china life sciences, 2020, 63(11):1768-1770. doi: 10.1007/s11427-020-1802-y
[54]	CHUCK GS, BROWN PJ, MEELEY R, et al. Maize SBP-box transcription factors unbranched2 and unbranched3 affect yield traits by regulating the rate of lateral primordia initiation[J]. Proceedings of the national academy of sciences, 2014, 111(52):18775-18780. doi: 10.1073/pnas.1407401112 URL
[55]	DOEBLEY J, STEC A, HUBBARD L. The evolution of apical dominance in maize[J]. Nature, 1997, 386(6624):485-488. doi: 10.1038/386485a0
[56]	BARBIER FF, DUN EA, KERR SC, et al. An update on the signals controlling shoot branching[J]. Trends in plant science, 2019, 24(3):220-236. doi: S1360-1385(18)30288-7 pmid: 30797425
[57]	SUN H, GUO X, QI X, et al. SPL14/17 act downstream of strigolactone signalling to modulate rice root elongation in response to nitrate supply[J]. Plant journal, 2021, 106(3):649-660. doi: 10.1111/tpj.v106.3 URL
[58]	SUN H, TAO J, LIU S, et al. Strigolactones are involved in phosphate- and nitrate-deficiency-induced root development and auxin transport in rice[J]. Journal of experimental botany, 2014, 65(22):6735-6746. doi: 10.1093/jxb/eru029 pmid: 24596173
[59]	YANG T, LIAN Y, KANG J, et al. The SUPPRESSOR of MAX2 1 (SMAX1)-Like SMXL6, SMXL7 and SMXL8 act as negative regulators in response to drought stress in arabidopsis[J]. Plant cell physiology, 2020, 61(8):1477-1492. doi: 10.1093/pcp/pcaa066 URL
[60]	LOU D, WANG H, LIANG G, et al. OsSAPK2 confers abscisic acid sensitivity and tolerance to drought stress in rice[J]. Frontiers in plant science, 2017, 8:993. doi: 10.3389/fpls.2017.00993 pmid: 28659944
[61]	LI W, NGUYEN K H, TRAN C D, et al. Negative roles of strigolactone-related SMXL6, 7 and 8 proteins in drought resistance in Arabidopsis[J]. Biomolecules, 2020, 10(4):607. doi: 10.3390/biom10040607 URL
[62]	孙卫健. 苹果独脚金内酯信号途径阻遏蛋白同源基因MdSMXL8.2的功能鉴定[D]. 泰安: 山东农业大学, 2020.