HD-Zip转录因子GhHB12通过调控生长素信号抑制棉花株高

doi:10.1016/j.jia.2022.09.022

摘要/Abstract

摘要：

陆地棉是世界上最重要的纤维作物。株高作为植物株型的重要组成部分，影响着作物的种植模式、产量和经济系数。前期研究中，我们分离并鉴定了一个棉花HD-ZIP基因（GhHB12），该基因调控棉花的非生物和生物胁迫应答反应和生长发育过程。在本研究中，我们证明GhHB12基因受生长素诱导表达，过表达GhHB12基因能激活HY5、ATH1和HAT4基因的表达，抑制生长素的时空分布、极性运输和信号传导，并改变细胞壁扩张相关基因的表达，最终抑制棉花株高。这些结果表明，GhHB12可以通过影响生长素的信号传导和细胞壁的扩展来调节棉花株高。

Abstract: Upland cotton (Gossypium hirsutum L.) is the most important natural textile fiber crop worldwide. Plant height (PH) is a significant component of plant architecture, strongly influencing crop cultivation patterns, overall yield, and economic coefficient. However, cotton genes regulating plant height have not been fully identified. Previously, an HD-Zip gene (GhHB12) was isolated and characterized in cotton, which regulates the abiotic and biotic stress responses and the growth and development processes. In this study, we showed that GhHB12 was induced by auxin. Moreover, overexpression of GhHB12 induces the expression of HY5, ATH1, and HAT4, represses the spatial-temporal distribution, polar transport, and signaling of auxin, alters the expression of genes involved in cell wall expansion, and restrains the plant height in cotton. These results suggest a role of GhHB12 in regulating cotton plant height, which could be achieved by affecting the auxin signaling and cell wall expansion.

Key words: cotton , GhHB12 , plant height , auxin , cell wall , HD-Zip

LIU Yan, WANG Wei-ping, ZHANG Lin, ZHU Long-fu, ZHANG Xian-long, HE Xin. HD-Zip转录因子GhHB12通过调控生长素信号抑制棉花株高[J]. Journal of Integrative Agriculture, 2023, 22(7): 2015-2024.

LIU Yan, WANG Wei-ping, ZHANG Lin, ZHU Long-fu, ZHANG Xian-long, HE Xin. The HD-Zip transcription factor GhHB12 represses plant height by regulating the auxin signaling in cotton[J]. Journal of Integrative Agriculture, 2023, 22(7): 2015-2024.

参考文献

Ang L H, Chattopadhyay S, Wei N, Oyama T, Okada K, Batschauer A, Deng X W. 1998. Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of arabidopsis development. Molecular Cell, 1, 213–222.

Brewer P B, Koltai H, Beveridge C A. 2013. Diverse roles of strigolactones in plant development. Molecular Plant, 6, 18–28.

Castorina G Consonni G. 2020. The role of brassinosteroids in controlling plant height in poaceae: A genetic perspective. International Journal of Molecular Sciences, 21, 1191.

Chae K, Isaacs C G, Reeves P H, Maloney G S, Muday G K, Nagpal P, Reed J W. 2012. Arabidopsis SMALL AUXIN UP RNA63 promotes hypocotyl and stamen filament elongation. The Plant Journal, 71, 684–697.

Chattopadhyay S, Ang L H, Puente P, Deng X W, Wei N. 1998. Arabidopsis bZIP protein HY5 directly interacts with light-responsive promoters in mediating light control of gene expression. The Plant Cell, 10, 673–683.

Chen Y, Fan X, Song W, Zhang Y, Xu G. 2012. Over-expression of OsPIN2 leads to increased tiller numbers, angle and shorter plant height through suppression of OsLAZY1. Plant Biotechnology Journal, 10, 139–149.

Dai Z, Wang J, Yang X, Lu H, Miao X, Shi Z. 2018. Modulation of plant architecture by the miR156f-OsSPL7-OsGH3.8 pathway in rice. Journal of Experimental Botany, 69, 5117–5130.

Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, Ehrismann J S, Jürgens G, Estelle M. 2005. Plant development is regulated by a family of auxin receptor F box proteins. Developmental Cell, 9, 109–119.

Feng L, Chi B J, Dong H Z. 2022. Cotton cultivation technology with Chinese characteristics has driven the 70-year development of cotton production in China. Journal of Integrative Agriculture, 21, 597–609.

Fu C, Sunkar R, Zhou C, Shen H, Zhang J Y, Matts J, Wolf J, Mann D G, Stewart Jr C N, Tang Y, Wang Z Y. 2012. Overexpression of miR156 in switchgrass (Panicum virgatum L.) results in various morphological alterations and leads to improved biomass production. Plant Biotechnology Journal, 10, 443–452.

Fu Y Y, Win P, Zhang H J, Li C F, Shen Y, He F, Luo K M. 2019. PtrARF2.1 is involved in regulation of leaf development and lignin biosynthesis in poplar trees. International Journal of Molecular Sciences, 20, 4141.

Fukui K, Hayashi K I 2018. Manipulation and sensing of auxin metabolism, transport and signaling. Plant & Cell Physiology, 59, 1500–1510.

Gallavotti A. 2013. The role of auxin in shaping shoot architecture. Journal of Experimental Botany, 64, 2593–2608.

Gomez-Mena C, Sablowski R. 2008. ARABIDOPSIS THALIANA HOMEOBOX GENE1 establishes the basal boundaries of shoot organs and controls stem growth. The Plant Cell, 20, 2059–2072.

Guilfoyle T J, Hagen G. 2007. Auxin response factors. Current Opinion in Plant Biology, 10, 453–460.

Guo F, Huang Y Z, Qi P P, Lian G W, Hu X M, Han N, Wang J H, Zhu M Y, Qian Q, Bian H W. 2021. Functional analysis of auxin receptor OsTIR1/OsAFB family members in rice grain yield, tillering, plant height, root system, germination, and auxinic herbicide resistance. The New Phytologist, 229, 2676–2692.

He G, Liu P, Zhao H, Sun J. 2020. The HD-ZIP II transcription factors regulate plant architecture through the auxin pathway. International Journal of Molecular Sciences, 21, 3250.

He P, Zhang H Z, Zhang L, Jiang B, Xiao G H, Yu J N. 2022. The GhMAX2 gene regulates plant growth and fiber development in cotton. Journal of Integrative Agriculture, 21, 1563–1575.

He X, Luo X Y, Wang T Y, Liu S M, Zhang X L, Zhu L F. 2020. GhHB12 negatively regulates abiotic stress tolerance in Arabidopsis and cotton. Environmental and Experimental Botany, 176, 104087.

He X, Wang T Y, Xu Z, Liu N, Wang L C, Hu Q, Luo X Y, Zhang X L, Zhu L F. 2018a. The cotton HD-Zip transcription factor GhHB12 regulates flowering time and plant architecture via the GhmiR157-GhSPL pathway. Communications Biology, 1, 229.

He X, Wang T Y, Zhu W, Wang Y J, Zhu L F. 2018b. GhHB12, a HD-ZIP i transcription factor, negatively regulates the cotton resistance to Verticillium dahliae. International Journal of Molecular Sciences, 19, 3997.

Ji G, Liang C, Cai Y, Pan Z, Meng Z, Li Y, Jia Y, Miao Y, Pei X, Gong W, Wang X, Gao Q, Peng Z, Wang L, Sun J, Geng X, Wang P, Chen B, Wang P, Zhu T, et al. 2021. A copy number variant at the HPDA-D12 locus confers compact plant architecture in cotton. The New Phytologist, 229, 2091–2103.

Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X, Qian Q, Li J. 2010. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nature Genetics, 42, 541–544.

Kim J I, Bae D, Park H C, Chun H J, Oh D H, Lee M. K, Cha J Y, Kim W Y, Kim M C, Chung W S, Bohnert H J, Lee S Y, Bressan R A, Lee S W, Yun D J. 2013. Overexpression of Arabidopsis YUCCA6 in potato results in high-auxin developmental phenotypes and enhanced resistance to water deficit. Molecular Plant, 6, 337–349.

Li F, Yan D, Gao L F, Liu P, Zhao G Y, Jia J Z, Ren Z L. 2022. TaIAA15 genes regulate plant architecture in wheat. Journal of Integrative Agriculture, 21, 1243–1252.

Li H, Li J, Song J, Zhao B, Guo C, Wang B, Zhang Q, Wang J, King G J, Liu K. 2019. An auxin signaling gene BnaA3.IAA7 contributes to improved plant architecture and yield heterosis in rapeseed. The New Phytologist, 222, 837–851.

Liu H, Li X, Xiao J, Wang S. 2012. A convenient method for simultaneous quantification of multiple phytohormones and metabolites: Application in study of rice–bacterium interaction. Plant Methods, 8, 2.

Liu J, Cheng X, Liu P, Sun J. 2017. miR156-targeted SBP-box transcription factors interact with DWARF53 to regulate TEOSINTE BRANCHED1 and BARREN STALK1 expression in bread wheat. Plant Physiology, 174, 1931–1948.

Liu N, Tu L, Wang L, Hu H, Xu J, Zhang X. 2017. MicroRNA 157-targeted SPL genes regulate floral organ size and ovule production in cotton. BMC Plant Biology, 17, 7.

Lu G, Coneva V, Casaretto J A, Ying S, Mahmood K, Liu F, Nambara E, Bi Y M, Rothstein S J. 2015. OsPIN5b modulates rice (Oryza sativa) plant architecture and yield by changing auxin homeostasis, transport and distribution. The Plant Journal, 83, 913–925.

Ma J J, Pei W F, Ma Q F, Geng Y H, Liu G Y, Liu J, Cui Y P, Zhang X, Wu M, Li X.L, Li D, Zang X S, Song J K, Tang S R, Zhang J F, Yu S X, Yu J W. 2019. QTL analysis and candidate gene identification for plant height in cotton based on an interspecific backcross inbred line population of Gossypium hirsutum×Gossypium barbadense. Theoretical and Applied Genetics, 13, 2663–2676.

Ma Q, Grones P, Robert S. 2018. Auxin signaling: A big question to be addressed by small molecules. Journal of Experimental Botany, 69, 313–328.

Majda M, Robert S. 2018. The role of auxin in cell wall expansion. International Journal of Molecular Sciences, 19, 951.

Miura K, Ikeda M, Matsubara A, Song X J, Ito M, Asano K, Matsuoka M, Kitano H, Ashikari M. 2010. OsSPL14 promotes panicle branching and higher grain productivity in rice. Nature Genetics, 42, 545–549.

Nagpal P, Walker L M, Young J C, Sonawala A, Timpte C, Estelle M, Reed J W. 2000. AXR2 encodes a member of the Aux/IAA protein family. Plant Physiology, 123, 563–574.

Peng J, Richards D E, Hartley N M, Murphy G P, Devos K M, Flintham J E, Beales J, Fish L J, Worland A J, Pelica F, Sudhakar D, Christou P, Snape J W, Gale M D, Harberd N P. 1999. ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature, 400, 256–261.

Perrot-Rechenmann C. 2010. Cellular responses to auxin: Division versus expansion. Cold Spring Harbor Perspectives in Biology, 2, a001446.

Piao R, Chu S H, Jiang W, Yu Y, Jin Y, Woo M O, Lee J, Kim S, Koh H J. 2014. Isolation and characterization of a dominant dwarf gene, d-h, in rice. PLoS ONE, 9, e86210.

Qanmber G, Lu L, Liu Z, Yu D, Zhou K, Huo P, Li F, Yang Z. 2019. Genome-wide identification of GhAAI genes reveals that GhAAI66 triggers a phase transition to induce early flowering. Journal of Experimental Botany, 70, 4721–4736.

Quaedvlieg N, Dockx J, Rook F, Weisbeek P, Smeekens S. 1995. The homeobox gene ATH1 of Arabidopsis is derepressed in the photomorphogenic mutants cop1 and det1. The Plant Cell, 7, 117–129.

Sannemann W, Lisker A, Maurer A, Leon J, Kazman E, Coster H, Holzapfel J, Kempf H, Korzun V, Ebmeyer E, Pillen K. 2018. Adaptive selection of founder segments and epistatic control of plant height in the MAGIC winter wheat population WM-800. BMC Genomics, 19, 559.

Sasaki A, Ashikari M, Ueguchi-Tanaka M, Itoh H, Nishimura A, Swapan D, Ishiyama K, Saito T, Kobayashi M, Khush G S, Kitano H, Matsuoka M. 2002. Green revolution: A mutant gibberellin-synthesis gene in rice. Nature, 416, 701–702.

Sauer M, Robert S, Kleine-Vehn J. 2013. Auxin: simply complicated. Journal of Experimental Botany, 64, 2565–2577.

Shang L G, Liu F, Wang Y M, Abduweli A, Cai S H, Wang K B, Hua J P. 2015. Dynamic QTL mapping for plant height in Upland cotton (Gossypium hirsutum). Plant Breeding, 134, 703–712.

Silverstone A L, Sun T. 2000. Gibberellins and the green revolution. Trends in Plant Science, 5, 1–2.

Song X L, Zhang T Z. 2009. Quantitative trait loci controlling plant architectural traits in cotton. Plant Science, 177, 317–323.

Sun Z, Su C, Yun J, Jiang Q, Wang L, Wang Y, Cao D, Zhao F, Zhao Q, Zhang M, Zhou B, Zhang L, Kong F, Liu B, Tong Y, Li X. 2019. Genetic improvement of the shoot architecture and yield in soya bean plants via the manipulation of GmmiR156b. Plant Biotechnology Journal, 17, 50–62.

Udvardi M K, Scheible W R. 2005. Plant science. GRAS genes and the symbiotic green revolution. Science, 308, 1749–1750.

Wang B, Smith S M, Li J. 2018. Genetic regulation of shoot architecture. Annual Review of Plant Biology, 69, 437–468.

Wang J W, Czech B, Weigel D. 2009. miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell, 138, 738–749.

Wang L, Sun S, Jin J, Fu D, Yang X, Weng X, Xu C, Li X, Xiao J, Zhang Q. 2015. Coordinated regulation of vegetative and reproductive branching in rice. Proceedings of the National Academy of Sciences of the United States of America, 112, 15504–15509.

Xu Y X, Xiao M Z, Liu Y, Fu J L, He Y, Jiang D A. 2017. The small auxin-up RNA OsSAUR45 affects auxin synthesis and transport in rice. Plant Molecular Biology, 94, 97–107.

Yamamoto Y, Kamiya N, Morinaka Y, Matsuoka M, Sazuka T. 2007. Auxin biosynthesis by the YUCCA genes in rice. Plant physiology, 143, 1362–1371.

Yan W, Du M W, Zhao W C, Li F, Wang X R, Eneji A E, Yang F Q, Huang J, Meng L, Qi H K, Xue G J, Xu D Y, Tian X L, Li Z H. 2019. Relationships between plant architecture traits and cotton yield within the plant height range of 80–120 cm desired for mechanical harvesting in the yellow river valley of China. Agronomy-Basel, 9, 587.

Yang Z, Zhang C, Yang X, Liu K, Wu Z, Zhang X, Zheng W, Xun Q, Liu C, Lu L, Yang Z, Qian Y, Xu Z, Li C, Li J, Li F. 2014. PAG1, a cotton brassinosteroid catabolism gene, modulates fiber elongation. The New Phytologist, 203, 437–448.

Zhang T, Hu Y, Jiang W, Fang L, Guan X, Chen J, Zhang J, Saski C A, Scheffler B E, Stelly D M, Hulse-Kemp A M, Wan Q, Liu B, Liu C, Wang S, Pan M, Wang Y, Wang D, Ye W, Chang L, et al. 2015. Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nature Biotechnology, 33, 531–537.

Zhu L F, He X, Yuan D J, Xu L A, Xu L, Tu L L, Shen G X, Zhang H, Zhang X L. 2011. Genome-wide identification of genes responsive to ABA and cold/salt stresses in Gossypium hirsutum by data-mining and expression pattern analysis. Agricultural Sciences in China, 10, 499–508.