BTA2 regulates tiller angle and the shoot gravity response through controlling auxin content and distribution in rice

Abstract

Tiller angle is a key agricultural trait that establishes plant architecture, which in turn strongly affects grain yield by influencing planting density in rice. The shoot gravity response plays a crucial role in the regulation of tiller angle in rice, but the underlying molecular mechanism is largely unknown. Here, we report the identification of the BIG TILLER ANGLE2 (BTA2), which regulates tiller angle by controlling the shoot gravity response in rice. Loss-of-function mutation of BTA2 dramatically reduced auxin content and affected auxin distribution in rice shoot base, leading to impaired gravitropism and therefore a big tiller angle. BTA2 interacted with AUXIN RESPONSE FACTOR7 (ARF7) to modulate rice tiller angle through the gravity signaling pathway. The BTA2 protein was highly conserved during evolution. Sequence variation in the BTA2 promoter of indica cultivars harboring a less expressed BTA2 allele caused lower BTA2 expression in shoot base and thus wide tiller angle during rice domestication. Overexpression of BTA2 significantly increased grain yield in the elite rice cultivar Huanghuazhan under appropriate dense planting conditions. Our findings thus uncovered the BTA2-ARF7 module that regulates tiller angle by mediating the shoot gravity response. Our work offers a target for genetic manipulation of plant architecture and valuable information for crop improvement by producing the ideal plant type.

Keywords

auxin / domestication / gravity response / rice / tiller angle

References

[1] Bailey, T.L.,Johnson, J.,Grant, C.E., and Noble, W.S. (2015). The meme suite. Nucleic Acids Res. 43:39–49.

[2] Cai, Y.,Huang, L.,Song, Y.,Yuan, Y.,Xu, S.,Wang, X.,Liang, Y.,Zhou, J.,Liu, G.,Li, J., et al. (2023). LAZY3 interacts with LAZY2 to regulate tiller angle by modulating shoot gravity perception in rice. Plant Biotechnol. J. 21:1217–1228.

[3] Cao, R.,Zhao, S.,Jiao, G.,Duan, Y.,Ma, L.,Dong, N.,Lu, F.,Zhu, M.,Shao, G.,Hu, P., et al. (2022). OPAQUE3, encoding a transmembrane bZIP transcription factor, regulates endosperm storage protein and starch biosynthesis in rice. Plant Comm. 3:100463.

[4] Chawla, M.,Verma, V.,Kapoor, M., and Kapoor, S. (2017). A novel application of periodic acid–Schiff (PAS) staining and fluorescence imaging for analysing tapetum and microspore development. Histochem. Cell Biol. 147:103–110.

[5] Chen, C.,Chen, H.,Zhang, Y.,Thomas, H.R.,Frank, M.H.,He, Y., and Xia, R. (2020). TBtools: An integrative toolkit developed for interactive analyses of big biological data. Mol. Plant 13:1194–1202.

[6] Chen, J.,Yu, R.,Li, N.,Deng, Z.,Zhang, X.,Zhao, Y.,Qu, C.,Yuan, Y.,Pan, Z.,Zhou, Y., et al. (2023). Amyloplast sedimentation repolarizes LAZYs to achieve gravity sensing in plants. Cell 186:4788–4802.

[7] Chen, S.B.,Tao, L.Z.,Zeng, L.R.,Vega-Sanchez, M.,Umemura, K., and Wang, G.L. (2006). A highly efficient transient protoplast system for analyzing defence gene expression and protein-protein interactions in rice. Mol. Plant Pathol. 7:417–427.

[8] Chen, W.K.,Chen, L.,Zhang, X.,Yang, N.,Guo, J.H.,Wang, M.,Ji, S.H.,Zhao, X.Y.,Yin, P.F.,Cai, L.C., et al. (2022). Convergent selection of a WD40 protein that enhances grain yield in maize and rice. Science 375:eabg7985.

[9] Chen, Y.,Fan, X.,Song, W.,Zhang, Y., and Xu, G. (2012). Over-expression of OsPIN2 leads to increased tiller numbers, angle and shorter plant height through suppression of OsLAZY1. Plant Biotechnol. J. 10:139–149.

[10] Danecek, P.,Auton, A.,Abecasis, G.,Albers, C.A.,Banks, E.,DePristo, M.A.,Handsaker, R.E.H.,Lunter, G.,Marth, G.T.,Sherry, S.T., et al. (2011). The variant call format and VCFtools. Bioinformatics 27:2156–2158.

[11] Ding, C.,Lin, X.,Zuo, Y.,Yu, Z.,Baerson, S.R.,Pan, Z.,Zeng, R., and Song, Y. (2021). Transcription factor OsbZIP49 controls tiller angle and plant architecture through the induction of indole-3-acetic acid-amido synthetases in rice. Plant J. 108:1346–1364.

[12] Dong, H.,Zhao, H.,Xie, W.,Han, Z.,Li, G.,Yao, W.,Bai, X.,Hu, Y.,Guo, Z.,Lu, K., et al. (2016). A novel tiller angle gene,TAC3, together with TAC1 and D2 largely determine the natural variation of tiller angle in rice cultivars. PLoS Genet. 12:e1006412.

[13] Gao, H.,Wang, W.,Wang, Y., and Liang, Y. (2019). Molecular mechanisms underlying plant architecture and its environmental plasticity in rice. Mol. Breed. 39:167.

[14] Hiei, Y., and Komari, T. (2008). Agrobacterium-mediated transformation of rice using immature embryos or calli induced from mature seed. Nat. Protoc. 3:824–834.

[15] Hu, M.,Lv, S.,Wu, W.,Fu, Y.,Liu, F.,Wang, B.,Li, W.,Gu, P.,Cai, H.,Sun, C., et al. (2018). The domestication of plant architecture in African rice. Plant J. 94:661–669.

[16] Hu, Y.,Li, S.,Fan, X.,Song, S.,Zhou, X.,Weng, X.,Xiao, J.,Li, X.,Xiong, L.,You, A., et al. (2020). OsHOX1 and OsHOX28 redundantly shape rice tiller angle by reducing HSFA2D expression and auxin content. Plant Physiol. 184:1424–1437.

[17] Huang, G.,Hu, H.,van de Meene, A.,Zhang, J.,Dong, L.,Zheng, S.,Zhang, F.,Betts, N.,Liang, W.,Bennett, M., et al. (2021a). AUXIN RESPONSE FACTORS 6 and 17 control the flag leaf angle in rice by regulating secondary cell wall biosynthesis of lamina joints. Plant Cell 33:3120–3133.

[18] Huang, L.,Wang, W.,Zhang, N.,Cai, Y.,Liang, Y.,Meng, X.,Yuan, Y.,Li, J.,Wu, D., and Wang, Y. (2021b). LAZY2 controls rice tiller angle through regulating starch biosynthesis in gravity-sensing cells. New Phytol. 231:1073–1087.

[19] Jefferson, R.A.,Kavanagh, T.A., and Bevan, M.W. (1987). GUS fusions: Betaglucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6:3901–3907.

[20] Jiang, J.,Tan, L.,Zhu, Z.,Fu, Y.,Liu, F.,Cai, H., and Sun, C. (2012). Molecular evolution of the TAC1 gene from rice (Oryza sativa L.). J. Genet. Genomics 39:551–560.

[21] Jin, J.,Huang, W.,Gao, J.P.,Yang, J.,Shi, M.,Zhu, M.Z.,Luo, D., and Lin, H.X. (2008). Genetic control of rice plant architecture under domestication. Nat. Genet. 40:1365–1369.

[22] Johnson, M.,Zaretskaya, I.,Raytselis, Y.,Merezhuk, Y.,McGinnis, S., and Madden, T.L. (2008). NCBI blast: A better web interface. Nucleic Acids Res. 36:5–9.

[23] Khush, G.S. (2013). Strategies for increasing the yield potential of cereals: Case of rice as an example. Plant Breed. 132:433–436.

[24] Li, G.,Liang, W.,Zhang, X.,Ren, H.,Hu, J.,Bennett, M.J., and Zhang, D. (2014). Rice actin-binding protein RMD is a key link in the auxin-actin regulatory loop that controls cell growth. Proc. Natl. Acad. Sci. U.S.A. 111:10377–10382.

[25] Li, H.,Sun, H.,Jiang, J.,Sun, X.,Tan, L., and Sun, C. (2021). TAC4 controls tiller angle by regulating the endogenous auxin content and distribution in rice. Plant Biotechnol. J. 19:64–73.

[26] Li, P.,Wang, Y.,Qian, Q.,Fu, Z.,Wang, M.,Zeng, D.,Li, B.,Wang, X., and Li, J. (2007). LAZY1 controls rice shoot gravitropism through regulating polar auxin transport. Cell Res. 17:402–410.

[27] Li, Y.,Han, S., and Qi, Y. (2023). Advances in structure and function of auxin response factor in plants. J. Integr. Plant Biol. 65:617–632.

[28] Li, Y.,Li, J.,Chen, Z.,Wei, Y.,Qi, Y., and Wu, C. (2020). OsmiR167a-targeted auxin response factors modulate tiller angle via fine-tuning auxin distribution in rice. Plant Biotechnol. J. 18:2015–2026.

[29] Li, Y.,Zhu, J.,Wu, L.,Shao, Y.,Wu, Y., and Mao, C. (2019a). Functional divergence of PIN1 paralogous genes in rice. Plant Cell Physiol. 60:2720–2732.

[30] Li, Z.,Liang, Y.,Yuan, Y.,Wang, L.,Meng, X.,Xiong, G.,Zhou, J.,Cai, Y.,Han, N.,Hua, L., et al. (2019b). OsBRXL4 regulates shoot gravitropism and rice tiller angle through affecting LAZY1 nuclear localization. Mol. Plant 12:1143–1156.

[31] Liu, K., and Muse, S.V. (2005). Power Marker: An integrated analysis environment for genetic marker analysis. Bioinformatics 21:2128–2129.

[32] Morita, M.T., and Tasaka, M. (2004). Gravity sensing and signaling. Curr. Opin. Plant Biol. 7:712–718.

[33] Nakamura, M.,Nishimura, T., and Morita, M.T. (2019). Gravity sensing and signal conversion in plant gravitropism. J. Exp. Bot. 70:3495–3506.

[34] Okamura, M.,Hirose, T.,Hashida, Y.,Yamagishi, T.,Ohsugi, R., and Aoki, N. (2013). Starch reduction in rice stems due to a lack of OsAGPL1 or OsAPL3 decreases grain yield under low irradiance during ripening and modifies plant architecture. Funct. Plant Biol. 40:1137–1146.

[35] 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., et al. (1999). ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400:256–261.

[36] Qi, Y.,Wang, S.,Shen, C.,Zhang, S.,Chen, Y.,Xu, Y.,Liu, Y.,Wu, Y., and Jiang, D. (2012). OsARF12, a transcription activator on auxin response gene, regulates root elongation and affects iron accumulation in rice (Oryza sativa). New Phytol. 193:109–120.

[37] Sack, F.D. (1991). Plant gravity sensing. Int. Rev. Cytol. 127:193–252.

[38] Sack, F.D. (1997). Plastids and gravitropic sensing. Planta 203:63–68.

[39] Sakuraba, Y.,Piao, W.,Lim, J.H.,Han, S.H.,Kim, Y.S.,An, G., and Paek, N.C. (2015). Rice ONAC106 inhibits leaf senescence and increases salt tolerance and tiller angle. Plant Cell Physiol. 56:2325–2339.

[40] Sang, D.,Chen, D.,Liu, G.,Liang, Y.,Huang, L.,Meng, X.,Chu, J.,Sun, X.,Dong, G.,Yuan, Y., et al. (2014). Strigolactones regulate rice tiller angle by attenuating shoot gravitropism through inhibiting auxin biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 111:11199–11204.

[41] Sasaki, A.,Ashikari, M.,Ueguchi-Tanaka, M.,Itoh, H.,Nishimura, A.,Swapan, D.,Ishiyama, K.,Saito, T.,Kobayashi, M.,Khush, G.S., et al. (2002). A mutant gibberellin-synthesis gene in rice. Nature 416:701–702.

[42] Shang, L.G.,Li, X.X.,He, H.Y.,Yuan, Q.L.,Song, Y.N.,Wei, Z.R.,Lin, H.,Hu, M.,Zhao, F.L.,Zhang, C., et al. (2022). A super pan-genomic landscape of rice. Cell Res. 32:878–896.

[43] Shen, C.J.,Wang, S.K.,Bai, Y.H.,Wu, Y.R.,Zhang, S.N.,Chen, M.,Guilfoyle, T.J.,Wu, P., and Qi, Y.H. (2010). Functional analysis of the structural domain of ARF proteins in rice (Oryza sativa L.). J. Exp. Bot. 61:3971–3981.

[44] Song, X.,Xiong, Y.,Kong, X., and Huang, G. (2023). Roles of auxin response factors in rice development and stress responses. Plant Cell Environ. 46:1075–1086.

[45] Spielmeyer, W.,Ellis, M.H., and Chandler, P.M. (2002). Semidwarf (sd-1), “green revolution” rice, contains a defective gibberellin 20-oxidase gene. Proc. Natl. Acad. Sci. U.S.A. 99:9043–9048.

[46] Tamura, K.,Stecher, G., and Kumar, S. (2021). Mega11: Molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 38:3022–3027.

[47] Tan, L.,Li, X.,Liu, F.,Sun, X.,Li, C.,Zhu, Z.,Fu, Y.,Cai, H.,Wang, X.,Xie, D., et al. (2008). Control of a key transition from prostrate to erect growth in rice domestication. Nat. Genet. 40:1360–1364.

[48] Ulmasov, T.,Hagen, G., and Guilfoyle, T.J. (1997). ARF1, a transcription factor that binds to auxin response elements. Science 276:1865–1868.

[49] Ulmasov, T.,Hagen, G., and Guilfoyle, T.J. (1999). Activation and repression of transcription by auxin-response factors. Proc. Natl. Acad. Sci. U.S.A. 96:5844–5849.

[50] Wang, C.,Shen, L.,Fu, Y.,Yan, C., and Wang, K. (2015). A simple CRISPR/Cas9 system for multiplex genome editing in rice. J. Genet. Genomics 42:703–706.

[51] Wang, D.,Pei, K.,Fu, Y.,Sun, Z.,Li, S.,Liu, H.,Tang, K.,Han, B., and Tao, Y. (2007). Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa). Gene 394:13–24.

[52] Wang, W.,Gao, H.,Liang, Y.,Li, J., and Wang, Y. (2022). Molecular basis underlying rice tiller angle: Current progress and future perspectives. Mol. Plant 15:125–137.

[53] Wang, W.,Mauleon, R.,Hu, Z.Q.,Chebotarov, D.,Tai, S.S.,Wu, Z.C.,Li, M.,Zheng, T.Q.,Fuentes, R.R.,Zhang, F., et al. (2018). Genomic variation in 3, 010 diverse accessions of Asian cultivated rice. Nature 557:43–49.

[54] Wang, Y., and Li, J. (2008). Molecular basis of plant architecture. Annu. Rev. Plant Biol. 59:253–279.

[55] Wu, X.,Tang, D.,Li, M.,Wang, K., and Cheng, Z. (2013). Loose Plant Architecture1, an indeterminate domain protein involved in shoot gravitropism, regulates plant architecture in rice. Plant Physiol. 161:317–329.

[56] Wu, Y.,Zhao, S.,Li, X.,Zhang, B.,Jiang, L.,Tang, Y.,Zhao, J.,Ma, X.,Cai, H.,Sun, C., et al. (2018). Deletions linked to PROG1 gene participate in plant architecture domestication in Asian and African rice. Nat. Commun. 9:4157.

[57] Xu, Y.,McCouch, S.R., and Shen, Z. (1998). Transgressive segregation of tiller angle in rice caused by complementary gene action. Crop Sci. 38:12–19.

[58] Ye, J.,Zhang, M.,Yuan, X.,Hu, D.,Zhang, Y.,Xu, S.,Li, Z.,Li, R.,Liu, J.,Sun, Y., et al. (2022). Genomic insight into genetic changes and shaping of major inbred rice cultivars in China. New Phytol. 236:2311–2326.

[59] Yoshihara, T., and Iino, M. (2007). Identification of the gravitropism-related rice gene LAZY1 and elucidation of LAZY1-dependent and -independent gravity signaling pathways. Plant Cell Physiol. 48:678–688.

[60] Yu, B.,Lin, Z.,Li, H.,Li, X.,Li, J.,Wang, Y.,Zhang, X.,Zhu, Z.,Zhai, W.,Wang, X., et al. (2007). TAC1, a major quantitative trait locus controlling tiller angle in rice. Plant J. 52:891–898.

[61] Yu, J.P.,Miao, J.L.,Zhang, Z.Y.,Xiong, H.Y.,Zhu, X.Y.,Sun, X.M.,Pan, Y.H.,Liang, Y.T.,Zhang, Q.,Rehman, R.M.A., et al. (2018). Alternative splicing of OsLG3b controls grain length and yield in japonica rice. Plant Biotechnol. J. 16:1667–1678.

[62] Zhang, N.,Yu, Hong, Yu, Hao, Cai, Y.,Huang, L.,Xu, C.,Xiong, G.,Meng, X.,Wang, J.,Chen, H., et al. (2018). A core regulatory pathway controlling rice tiller angle mediated by the LAZY1-dependent asymmetric distribution of auxin. Plant Cell 30:1461–1475.

[63] Zhang, W.,Tan, L.,Sun, H.,Zhao, X.,Liu, F.,Cai, H.,Fu, Y.,Sun, X.,Gu, P.,Zhu, Z., et al. (2019). Natural variations at TIG1 encoding a TCP transcription factor contribute to plant architecture domestication in rice. Mol. Plant 12:1075–1089.

[64] Zhang, Y., and Friml, J. (2020). Auxin guides roots to avoid obstacles during gravitropic growth. New Phytol. 225:1049–1052.

[65] Zhang, Z.Y.,Li, J.J.,Pan, Y.H.,Li, J.L.,Zhou, L.,Shi, H.L.,Zeng, Y.W.,Guo, H.F.,Yang, S.M.,Zheng, W.W., et al. (2017). Natural variation in CTB4a enhances rice adaptation to cold habitats. Nat. Commun. 8:14788.

[66] Zhao, L.,Tan, L.,Zhu, Z.,Xiao, L.,Xie, D., and Sun, C. (2015). PAY1 improves plant architecture and enhances grain yield in rice. Plant J. 83:528–536.

[67] Zhao, L.,Zheng, Y.,Wang, Y.,Wang, S.,Wang, T.,Wang, C.,Chen, Y.,Zhang, K.,Zhang, N.,Dong, Z., et al. (2022). A HST1-like gene controls tiller angle through regulating endogenous auxin in common wheat. Plant Biotechnol. J. 22:122–135.

[68] Zhao, Q.,Ye, Y.,Han, Z.,Zhou, L.,Guan, X.,Pan, G.,Asad, M., and Cheng, F. (2020). SSIIIa-RNAi suppression associated changes in rice grain quality and starch biosynthesis metabolism in response to high temperature. Plant Sci. 294:110443.

[69] Zhao, Y.,Christensen, S.K.,Fankhauser, C.,Cashman, J.R.,Cohen, J.D.,Weigel, D., and Chory, J. (2001). A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291:306–309.

[70] Zhu, M.,Hu, Y.,Tong, A.,Yan, B.,Lv, Y.,Wang, S.,Ma, W.,Cui, Z., and Wang, X. (2020). LAZY1 controls tiller angle and shoot gravitropism by regulating the expression of auxin transporters and signaling factors in rice. Plant Cell Physiol. 61:2111–2125.

RIGHTS & PERMISSIONS

2024 The Author(s). Journal of Integrative Plant Biology published by John Wiley & Sons Australia, Ltd on behalf of Institute of Botany, Chinese Academy of Sciences.