|
|
|
| Research Progresses on the Synthesis, Signaling Pathways and Physiological Functions of Strigolactones |
| CHEN Jing-Wen1,2, ZHANG Jun-Min3, LI Yan-Yan1, JI Jun1* |
1 Center for Agricultural Resources Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Shijiazhuang 050022, China;
2 University of Chinese Academy of Sciences, Beijing 100049, China;
3 Anxin County Agricultural Technology Workstation, Baoding 071600, China |
|
|
|
|
Abstract Strigolactones (SLs) is a newly identified class of phytohormones that strongly inhibit the formation of branches/tillers in plants, and plays an important role in the process of plant growth and development and stress resistance. With the further study of SLs synthesis and signal pathway, a series of genes have been identified that can be used to regulate plant type formation. In this review, discovery process, chemical structure, synthetic pathway, metabolic pathway, distribution and transport, signaling pathway, and its function in regulating plant growth and development of SLs were reviewed. At the same time, the development of this field was prospeced, and it was believed that the regulation of plant type, resistance and parasitism by SLs would become the focus of future research. This paper provides ideas and theoretical basis for establishing ideal plant type and breeding new varieties with high yield and stress resistance in the future.
|
|
Received: 07 March 2024
|
|
|
|
Corresponding Authors:
* jijun@sjziam.ac.cn
|
|
|
|
[1] 周慧文, 罗含敏, 熊发前, 等. 2024. 蔗糖对植物分枝调控的研究进展[J]. 农业生物技术学报, 32(2): 458-470.(Zhou H W, Luo H M, Xiong F Q, et al.2024. Research progresses on the regulation of sucrose on plant branching[J]. Journal of Agricultural Biotechnology, 32(2): 458-470.
[2] 周希萌, 付春, 马长乐, 等. 2021. 作物分枝的分子调控研究进展[J]. 生物技术通报, 37(3): 107-114.(Zhou X M, Fu C, Ma C L, et al.2021. Research progress of molecular regulation of branching of crops[J]. Biotechnology Bulletin, 37(3): 107-114.
[3] Abe S, Sado A, Tanaka K, et al.2014. Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro[J]. Proceedings of the National Academy of Sciences of the USA, 111(50): 18084-18089.
[4] Akiyama K, Matsuzaki K I, Hayashi H.2005. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi[J]. Nature, 435(7073): 824-827.
[5] Alder A, Jamil M, Marzorati M, et al.2012. The path from β-carotene to carlactone, a strigolactone-like plant hormone[J]. Science, 335(6074): 1348-1351.
[6] Andreo J B, Ruyter S C, Bouwmeester H J, et al.2015. Ecological relevance of strigolactones in nutrient uptake and other abiotic stresses, and in plant-microbe interactions below-ground[J]. Plant and Soil, 394(1-2): 1-19.
[7] Arite T, Iwata H, Ohshima K, et al.2007. DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice[J]. The Plant Journal, 51(6): 1019-1029.
[8] Arite T, Kameoka H, Kyozuka J.2011. Strigolactone positively controls crown root elongation in rice[J]. Journal of Plant Growth Regulation, 31(2): 165-172.
[9] Arite T, Umehara M, Ishikawa S, et al.2009. d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers[J]. Plant and Cell Physiology, 50(8): 1416-1424.
[10] Beveridge C A.2000. Long-distance signalling and a mutational analysis of branching in pea[J]. Plant Growth Regulation, 32(2-3): 193-203.
[11] Beveridge C A, Kyozuka J.2010. New genes in the strigolactone-related shoot branching pathway[J]. Current Opinion in Plant Biology, 13(1): 34-39.
[12] Booker J, Sieberer T, Wright W, et al.2005. MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone[J]. Developmental Cell, 8(4): 443-449.
[13] Borghi L, Kang J, Ko D, et al.2015. The role of ABCG-type ABC transporters in phytohormone transport[J]. Biochemical Society Transactions, 43(5): 924-930.
[14] Bouwmeester H J, Roux C, Lopez-Raez J A, et al.2007. Rhizosphere communication of plants, parasitic plants and AM fungi[J]. Trends in Plant Science, 12(5): 224-230.
[15] Brewer P B, Yoneyama K, Filardo F, et al.2016. LAteral branching oxidoreductase acts in the final stages of strigolactone biosynthesis in Arabidopsis[J]. Proceedings of the National Academy of Sciences of the USA, 113(22): 6301-6306.
[16] Brooks D W, Bevinakatti H S, Powell D R.1985. The absolute structure of (+)-Strigol[J]. Journal of Organic Chemistry, 50(20): 3779-3781.
[17] Brown R, Greenwood, A D, Johnson A W, et al.1952. The Orobanche germination factor. 3. concentration of the factor by counter current distribution[J]. Biochemical Journal, 52(4): 571-574.
[18] Brown R, Greenwood, A D, Johnson A W, et al.1951. The stimulant involved in the germination of Orobanche minor Sm. 1. assay technique and bulk preparation of the stimulant[J]. Biochemical Journal, 48(5): 559-564.
[19] Bunsick M, Toh S, Wong C, et al.2020. SMAX1-dependent seed germination bypasses GA signalling in Arabidopsis and Striga[J]. Nature Plants, 6(6): 646-652.
[20] Butler LG.1995. Chemical communication between the parasitic weed Striga and its crop host: A new dimension in allelochemistry[J]. Allelopathy Chapter, 12: 158-168.
[21] Cardinale F, Korwin Krukowski P, Schubert A, et al.2018. Strigolactones: Mediators of osmotic stress responses with a potential for agrochemical manipulation of crop resilience[J]. Journal of Experimental Botany, 69(9): 2291-2303.
[22] Carlsson G H, Hasse D, Cardinale F, et al.2018. The elusive ligand complexes of the DWARF14 strigolactone receptor[J]. Journal of Experimental Botany, 69(9): 2345-2354.
[23] Chen L, Zhao Y, Xu S, et al.2018. OsMADS57 together with OsTB1 coordinates transcription of its target OsWRKY94 and D14 to switch its organogenesis to defense for cold adaptation in rice[J]. New Phytologist, 218(1): 219-231.
[24] Chini A, Fonseca S, Fernández G, et al.2007. The JAZ family of repressors is the missing link in jasmonate signalling[J]. Nature, 448(7154): 666-671.
[25] Cook C E, Whichard L P, Turner B, et al.1966. Germination of witchweed (Striga lutea Lour.): Isolation and properties of a potent stimulant[J]. Science, 154(3751): 1189-1190.
[26] Cook C E, Whichard L P, Wall M E.1972. Germination stimulants. II. Structure of strigol , a potent seed germination stimulant for witchweed (Striga lutea Lour.)[J]. Journal of the American Chemical Society, 94(17): 6199-6200.
[27] Dejong M, George G, Ongaro V, et al.2014. Auxin and strigolactone signaling are required for modulation of Arabidopsis shoot branching by nitrogen supply[J]. Plant Physiology, 166(1): 384-395.
[28] Drummond R S M, MartíNez-SáNchez N M, Janssen B J, et al.2009. Petunia hybrida carotenoid cleavage dioxygenase7 is involved in the production of negative and positive branching signals in petunia[J]. Plant Physiology, 151(4): 1867-1877.
[29] Dun E A, Brewer P B, Beveridge C A.2009. Strigolactones: Discovery of the elusive shoot branching hormone[J]. Trends in Plant Science, 14(7): 364-372.
[30] Ejeta G, Gressel G.2007. Integrating New Technologies for Striga Control[M]. World Scientific Publishing Co. Pte. Ltd., Singapore, 33: 267-349.
[31] Fang Z, Ji Y, Hu J, et al.2020. Strigolactones and brassinosteroids antagonistically regulate the stability of the D53-OsBZR1 complex to determine FC1 expression in rice tillering[J]. Molecular Plant, 13(4): 586-597.
[32] Gomez-Roldan V, Fermas S, Brewer P B, et al.2008. Strigolactone inhibition of shoot branching[J]. Nature, 455(7210): 189-194.
[33] Gray W M, Kepinsld S, Rouse D, et al.2001. Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins[J]. Nature, 414(6861): 271-276.
[34] Gutjahr C, Gobbato E, Chio J, et al.2015. Rice perception of symbiotic arbuscular mycorrhizal fungi requires the karrikin receptor complex[J]. Science, 350(6267): 1521-1524.
[35] Hamiaux C, Drummond Revel S M, Janssen B J, et al.2012. DAD2 is an α/β hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone[J]. Current Biology, 22(21): 2032-2036.
[36] Jiang L, Liu X, Xiong G, et al.2013. DWARF 53 acts as a repressor of strigolactone signalling in rice[J]. Nature, 504(7480): 401-405.
[37] Joel D M, Hershenhorn J, Eizenberg H, et al.2007. Biology and management of weedy root parasites[J]. Horticultural Reviews, 33: 267-349.
[38] Kohlen W, Charnikhova T, Liu Q, et al.2011. 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 Physiology, 155(2): 974-987.
[39] Kretzschmar T, Kohlen W, Sasse J, et al.2012. A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching[J]. Nature, 483(7389): 341-344.
[40] Lin H, Wang R, Qian Q, et al.2009. DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth[J]. The Plant Cell, 21(5): 1512-1525.
[41] Liu R, Hou J, Li H, et al.2021. Association of TaD14-4D, a gene involved in strigolactone signaling, with yield contributing traits in wheat[J]. International Journal of Molecular Science, 22(7): 3748.
[42] Lu Z, Yu H, Xiong G, et al.2013. Genome-wide binding analysis of the transcription activator ideal plant architecture1 reveals a complex network regulating rice plant architecture[J]. The Plant Cell, 25(10): 3743-3759.
[43] Mitra D, Beatriz E G, Khoshru B, et al.2021. Impacts of arbuscular mycorrhizal fungi on rice growth, development, and stress management with a particular emphasis on strigolactone effects on root development[J]. Communications in Soil Science and Plant Analysis, 52(12): 1591-1621.
[44] Mori N, Sado A, Xie X, et al.2020. Chemical identification of 18-hydroxycarlactonoic acid as an LjMAX1 product and in planta conversion of its methyl ester to canonical and non-canonical strigolactones in Lotus japonicus[J]. Phytochemistry, 174: 112349-112365.
[45] Musselman L J.1980. The biology of striga orobanche and other root-parasitic weeds[J]. Annual Review of Phytopathology, 18: 463-489.
[46] Napoli C.1996. Highly branched phenotype of the petunia dad1-1 mutant is reversed by grafting[J]. Plant Physiology, 111(1): 27-37.
[47] Radoslava M, Kumkum R, Francel W A, et al.2005. The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway[J]. Plant Physiology, 139(2): 920-934.
[48] Rasmussen A, Mason M G, De Cuyper C, et al.2012. Strigolactones suppress adventitious rooting in Arabidopsis and pea[J]. Plant Physiology, 158(4): 1976-1987.
[49] Runyon J B, Mescher M C, Moraes C.2006. Volatile chemical cues guide host location and host selection by parasitic plants[J]. Science, 313(5795): 1964-1967.
[50] Ruyter-Spira C, Kohlen W, Charnikhova T, et al.2011. Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: Another belowground role for strigolactones?[J]. Plant Physiology, 155(2): 721-734.
[51] Salim A B, Harro J B.2015. Strigolactones, a novel carotenoid-derived plant hormone[J]. Annual Review of Plant Biology, 66: 161-186.
[52] Sasse J, Simon S, Gübeli C, et al.2015. Asymmetric localizations of the abc transporter PaPDR1 trace paths of directional strigolactone transport[J]. Current Biology, 25(5): 647-655.
[53] Seto Y, Sado A, Asami K, et al.2014. Carlactone is an endogenous biosynthetic precursor for strigolactones[J]. Proceedings of the National Academy of Sciences, 111(4): 1640-1645.
[54] Seto Y.2024. Latest knowledge on strigolactone biosynthesis and perception[J]. Bioscience, Biotechnology, and Biochemistry, 88(1): 1-7.
[55] Siame B A, Weerasuriya Y, Wood K, et al.1993. Isolation of strigol, a germination stimulant for Striga asiatica, from host plants[J]. Journal of Agricultural and Food Chemistry, 41(9): 1486-1491.
[56] Simons J L, Napoli C A, Janssen B J, et al.2007. Analysis of the decreased apical dominance genes of petunia in the control of axillary branching[J]. Plant Physiology, 143(2): 697-706.
[57] Song X, Lu Z, Yu H, et al.2017. IPA1 functions as a downstream transcription factor repressed by D53 in strigolactone signaling in rice[J]. Cell Research, 27(9): 1128-1141.
[58] Stirnberg P, Furner I J, Ottoline Leyser H M.2007. MAX2 participates in an SCF complex which acts locally at the node to suppress shoot branching[J]. The Plant Journal, 50(1): 80-94.
[59] Stirnberg P, Sande K, Leyser O.2002. MAX1 and MAX2 control shoot lateral branching in Arabidopsis[J]. Development, 129(5): 1131-1141.
[60] Sun H, Guo X, Zhu X, et al.2023. Strigolactone and gibberellin signaling coordinately regulate metabolic adaptations to changes in nitrogen availability in rice[J]. Molecular Plant, 16(4): 588-598.
[61] Thines B, Katsir L, Melotto M, et al.2007. JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling[J]. Nature, 448(7154): 661-665.
[62] Ueda H, Kusaba M.2015. Strigolactone regulates leaf senescence in concert with ethylene in Arabidopsis[J]. Plant Physiology, 169(1): 138-147.
[63] Ueguchi-Tanaka M, Ashikari M, Nakajima M, et al.2005. Gibberellin insensitive dwarf1 encodes a soluble receptor for gibberellin[J]. Nature, 437(7059): 693-698.
[64] Umehara M, Hanada A, Magome H, et al.2010. Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice[J]. Plant and Cell Physiology, 51(7): 1118-1126.
[65] Umehara M, Hanada A, Yoshida S, et al.2008. Inhibition of shoot branching by new terpenoid plant hormones[J]. Nature, 455(7210): 195-200.
[66] Wang B, Smith S M, Li J.2018. Genetic regulation of shoot architecture[J]. Annual Review of Plant Biology, 69: 437-468.
[67] Wang L, Wang B, Jiang L, et al.2015. Strigolactone signaling in Arabidopsis regulates shoot development by targeting d53-like smxl repressor proteins for ubiquitination and degradation[J]. The Plant Cell, 27(11): 3128-3142.
[68] Wang L, Wang B, Yu H, et al.2020. Transcriptional regulation of strigolactone signalling in Arabidopsis[J]. Nature, 583(7815): 277-281.
[69] Wang X, Li Z, Shi Y, et al.2023. Strigolactones promote plant freezing tolerance by releasing the WRKY41‐mediated inhibition of CBF/DREB1 expression[J]. The EMBO Journal, 42(12): 112999-113015.
[70] Waters M T, Brewer P B, Bussell J D, et al.2012. The Arabidopsis ortholog of rice DWARF27 acts upstream of MAX1 in the control of plant development by strigolactones[J]. Plant Physiology, 159(3): 1073-1085.
[71] Xie X, Yoneyama K, Yoneyama K.2010. The strigolactone story[J]. Annual Review of Phytopathology, 48: 93-117.
[72] Xu E, Chai L, Zhang S, et al.2021. Catabolism of strigolactones by a carboxylesterase[J]. Nature Plants, 7(11): 1495-1504.
[73] Yamada Y, Furusawa S, Nagasaka S, et al.2014. Strigolactone signaling regulates rice leaf senescence in response to a phosphate deficiency[J]. Planta, 240(2): 399-408.
[74] Yamada Y, Umehara M.2015. Possible roles of strigolactones during leaf senescence[J]. Plants, 4(4): 664-677.
[75] Yao R, Ming Z, Yan L, et al.2016. DWARF14 is a non-canonical hormone receptor for strigolactone[J]. Nature, 536(7617): 469-473.
[76] Yoneyama K, Akiyama K, Brewer P B, et al.2020. Hydroxyl carlactone derivatives are predominant strigolactones in Arabidopsis[J]. Plant Direct, 4(1): 1-14.
[77] Yoshida S, Kameoka H, Tempo M, et al.2012. The D3 F‐box protein is a key component in host strigolactone responses essential for arbuscular mycorrhizal symbiosis[J]. New Phytologist, 196(4): 1208-1216.
[78] Yuan K, Zhang H, Yu C, et al.2023. Low phosphorus promotes NSP1-NSP2 heterodimerization to enhance strigolactone biosynthesis and regulate shoot and root architecture in rice[J]. Molecular Plant, 16(10): 1811-1831.
[79] Zhang Y, Dijk A D J, Adrian S, et al.2014. Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis[J]. Nature Chemical Biology, 10(12): 1025-1033.
[80] Zhao B, Wu T T, Ma S S, et al.2020. TaD27-B gene controls the tiller number in hexaploid wheat[J]. Plant Biotechnology Journal, 18(2): 513-525.
[81] Zhao L, Zhou X, Wu Z, et al.2013. Crystal structures of two phytohormone signal-transducing α/β hydrolases: Karrikin-signaling KAI2 and strigolactone-signaling DWARF14[J]. Cell Research, 23(3): 436-439.
[82] Zhou F, Lin Q, Zhu L, et al.2013. D14-SCFD3-dependent degradation of D53 regulates strigolactone signalling[J]. Nature, 504(7480): 406-410. |
|
|
|
