Abstract
Main conclusion
PROG1 is necessary but insufficient for the main culm inclination while TAC1 partially takes part in it, and both genes promote tiller inclination in Asian wild rice.
Abstract
Asian wild rice (Oryza rufipogon), the ancestor of cultivated rice (O. sativa), has a prostrate architecture, with tillers branching from near the ground. The main culm of each plant grows upward and then tilts during the vegetative stage. Genes controlling tiller angle have been reported; however, their genetic contributions to the culm movement have not been quantified. Here, we quantified their genetic contributions to angular kinematics in the main culm and tillers. For the main culm inclination, one major QTL surrounding the PROG1 region was found. In cultivated rice, tillers firstly inclined and lately rose, while it kept inclining in wild rice. It was suggested that PROG1 affected the tiller elevation angle in the later kinematics, whereas TAC1 was weakly associated with the tiller angle in the whole vegetative stage. Micro-computed tomography (micro-CT) suggested that these angular changes are produced by the bending of culm bases. Because near-isogenic lines (NILs) of wild rice-type Prog1 and Tac1 alleles in the genetic background of cultivated rice did not show the prostrate architecture, the involvement of another gene(s) for inclination of the main culm was suggested. Our findings will not only contribute to the understanding of the morphological transition during domestication but also be used in plant breeding to precisely reproduce the ideal plant architecture by combining the effects of multiple genes.
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Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
Abbreviations
- TAC1 :
-
TILLER ANGLE CONTROL 1
- PROG1 :
-
PROSTRATE GROWTH 1
- micro-CT:
-
Micro-computed tomography
- RIL:
-
Recombinant inbred line
- QTL:
-
Quantitative trait locus
References
Broman KW, Wu H, Sen Ś, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890. https://doi.org/10.1093/bioinformatics/btg112
Dardick C, Callahan A, Horn R, Ruiz KB, Zhebentyayeva T, Hollender C, Whitaker M, Abbott A, Scorza R (2013) PpeTAC1 promotes the horizontal growth of branches in peach trees and is a member of a functionally conserved gene family found in diverse plants species. Plant J 75:618–630. https://doi.org/10.1111/tpj.12234
Dong H, Zhao H, Han Z, Li G, Yao W, Bai X, Hu Y, Guo Z, Lu K, Yang L, Xing Y (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(11):e1006412. https://doi.org/10.1371/journal.pgen.1006412
González-Arcos M, de Noronha Fonceca ME, Zandonadi DB, Peres LEP, Arruabarrena A, Ferreira DS, Kevei Z, Mohareb F, Thompson AJ, Boiteux LS (2019) A loss-of-function allele of a TAC1-like gene (SlTAC1) located on tomato chromosome 10 is a candidate for the Erectoid leaf (Erl) mutation. Euphytica 215:95. https://doi.org/10.1007/s10681-019-2418-1
Hollender CA, Waite JM, Tabb A, Raines D, Chinnithambi DR, Dardick C (2018) Alteration of TAC1 expression in Prunus species leads to pleiotropic shoot phenotypes. Hortic Res 5:26. https://doi.org/10.1038/s41438-018-0034-1
Hollender CA, Hill JL Jr, Waite J, Dardick C (2020) Opposing influences of TAC1 and LAZY1 on lateral shoot orientation in Arabidopsis. Sci Rep 10:6051. https://doi.org/10.1038/s41598-020-62962-4
Hu Y, Li S, Fan X, Song S, Zhou X, Weng X, Xiao J, Li X, Xiong L, You A, Xing Y (2020) OsHOX1 and OsHOX28 redundantly shape rice tiller angle by reducing HSFA2D expression and auxin content. Plant Physiol 184:1424–1437. https://doi.org/10.1104/pp.20.00536
Huang X, Kurata N, Wei X et al (2012) A map of rice genome variation reveals the origin of cultivated rice. Nature 490:497–501. https://doi.org/10.1038/nature11532
Huang X, Yang S, Gong J, Zhao Q, Feng Q, Zhan Q, Zhao Y, Li Q, Cheng B, Xia J, Chen N, Huang T, Zhang L, Fan D, Chen J, Zhou C, Lu Y, Weng Q, Han B (2016) Genomic architecture of heterosis for yield traits in rice. Nature 537:629–633. https://doi.org/10.1038/nature19760
Inagaki N, Asami H, Hirabayashi H, Uchino A, Imaizumi T, Ishimaru K (2021) A rice ancestral genetic resource conferring ideal plant shapes for vegetative growth and weed suppression. Front Plant Sci 12:748531. https://doi.org/10.3389/fpls.2021.748531
Itoh J-I, Kitano H, Matsuoka M, Nagato Y (2000) SHOOT ORGANIZATION genes regulate shoot apical meristem organization and the pattern of leaf primordium initiation in rice. Plant Cell 12:2161–2174. https://doi.org/10.1105/tpc.12.11.2161
Jiang J, Tan L, Zhu Z, Fu Y, Liu F, Cai H, Sun C (2012) Molecular evolution of the TAC1 gene from rice (Oryza sativa L.). J Genet Genomes 39:551–560. https://doi.org/10.1016/j.jgg.2012.07.011
Jin J, Huang W, Gao J-P, Yang J, Shi M, Zhu M-Z, Lin H-X (2008) Genetic control of rice plant architecture under domestication. Nat Genet 40:1365–1369. https://doi.org/10.1038/ng.247
Ku L, Wei X, Zhang S, Zhang J, Guo S, Chen Y (2011) Cloning and characterization of a putative TAC1 ortholog associated with leaf angle in maize (Zea mays L.). PLoS ONE 6:e20621. https://doi.org/10.1371/journal.pone.0020621
Li Z, Paterson AH, Pinson SRM, Stansel JW (1999) RFLP facilitated analysis of tiller and leaf angles in rice (Oryza sativa L.). Euphytica 109:79–84. https://doi.org/10.1023/A:1003533001014
Li C, Zhou A, Sang T (2006) Genetic analysis of rice domestication syndrome with the wild annual species, Oryza nivara. New Phytol 170:185–194. https://doi.org/10.1111/j.1469-8137.2005.01647.x
Li P, Wang Y, Qian Q, Fu Z, Wang M, Zeng D, Li B, Wang X, Li J (2007) LAZY1 controls rice shoot gravitropism through regulating polar auxin transport. Cell Res 17:402–410. https://doi.org/10.1038/cr.2007.38
Li Y, Li J, Chen Z, Wei Y, Qi Y, Wu C (2020) OsmiR167a-targeted auxin response factors modulate tiller angle via fine-tuning auxin distribution in rice. Plant Biotechnol J 18:2015–2026. https://doi.org/10.1111/pbi.13360
Li H, Sun H, Jiang J, Sun X, Tan L, Sun C (2021) TAC4 controls tiller angle by regulating the endogenous auxin content and distribution in rice. Plant Biotechnol J 19:64–73. https://doi.org/10.1111/pbi.13440
Maeno A, Tsuda K (2018) Micro-computed tomography to visualize vascular networks in maize stems. Bio-Protocol. 8:1–18. https://doi.org/10.21769/2FBioProtoc.2682
Onishi K, Horiuchi Y, Ishigoh-Oka N, Takagi K, Ichikawa N, Maruoka M, Sano Y (2007) A QTL cluster for plant architecture and its ecological significance in Asian wild rice. Breeding Sci 57:7–16. https://doi.org/10.1270/jsbbs.57.7
Onishi K, Ichikawa N, Horiuchi Y, Kohara H, Sano Y (2018) Genetic architecture underlying the evolutionary change of competitive ability in Asian cultivated and wild rice. J Plant Interact 13(1):442–449. https://doi.org/10.1080/17429145.2018.1502821
Roychoudhry S, Kepinski S (2015) Shoot and root branch growth angle control—the wonderfulness of lateralness. Curr Opin Plant Biol 23:124–131. https://doi.org/10.1016/j.pbi.2014.12.004
Roychoudhry S, Del Bianco M, Kieffer M, Kepinski S (2013) Auxin controls gravitropic setpoint angle in higher plant lateral branches. Curr Biol 23:1497–1504. https://doi.org/10.1016/j.cub.2013.06.034
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez J-Y, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9(7):676–682. https://doi.org/10.1038/nmeth.2019
Song Y, Li G, Nowak J, Zhang X, Xu D, Yang X, Huang G, Liang W, Yang L, Wang C, Bulone V, Nikoloski Z, Hu J, Persson S, Zhang D (2019) The rice actin-binding protein RMD regulates light-dependent shoot gravitropism. Plant Physiol 181:630–644. https://doi.org/10.1104/pp.19.00497
Tan L, Li X, Liu F, Sun X, Li C, Zhu Z, Fu Y, Cai H, Wang X, Xie D, Sun C (2008) Control of a key transition from prostrate to erect growth in rice domestication. Nat Genet 40:1360–1364. https://doi.org/10.1038/ng.197
Taniguchi M, Furutani M, Nishimura T, Nakamura M, Fushita T, Iijima K, Baba K, Tanaka H, Toyota M, Tasaka M, Morita MT (2017) The Arabidopsis LAZY1 family plays a key role in gravity signaling within statocytes and in branch angle control of roots and shoots. Plant Cell 29:1984–1999. https://doi.org/10.1105/tpc.16.00575
Thomson MJ, Tai TH, McClung AM, Lai X-H, Hinga ME, Lobos KB, Xu Y, Martinez CP, McCouch SR (2003) Mapping quantitative trait loci for yield, yield components and morphological traits in an advanced backcross population between Oryza rufipogon and the Oryza sativa cultivar Jefferson. Theor Appl Genetics 107:479–493. https://doi.org/10.1007/s00122-003-1270-8
Tokuyama Y, Koide Y, Onishi K, Hikichi K, Omachi M, Takamure I, Kishima Y (2021) The mechanical origin of the radial shape in distichous phyllotaxy grass plants. In Silico Plants 3(2):diab019. https://doi.org/10.1093/insilicoplants/diab019
Waite JM, Dardick C (2018) TILLER ANGLE CONTROL 1 modulates plant architecture in response to photosynthetic signals. J Exp Bot 69:4935–4944. https://doi.org/10.1093/jxb/ery253
Waite JM, Dardick C (2020) IGT/LAZY family genes are differentially influenced by light signals and collectively required for light-induced changes to branch angle. bioRxiv. https://doi.org/10.1101/2020.07.15.205625
Wang L, Cai W, Du C, Fu Y, Xie X, Zhu Y (2018) The isolation of the IGT family genes in Malus × domestica and their expressions in four ideotype apple cultivars. Tree Genet Genomes 14:46. https://doi.org/10.1007/s11295-018-1258-9
Wang H, Tu R, Sun L, Wang D, Ruan Z, Zhang Y, Peng Z, Zhou X, Fu J, Liu Q, Wu W, Zhan X, Shen X, Zhang Y, Cao L, Cheng S (2022) Tiller Angle Control 1 is essential for the dynamic changes in plant architecture in rice. Int J Mol Sci 23:4997. https://doi.org/10.3390/ijms23094997
Wang H, Tu R, Ruan Z, Chen C, Peng Z, Zhou X, Sun L, Hong Y, Chen D, Liu Q, Wu W, Zhan X, Shen X, Zhou Z, Cao L, Zhang Y, Cheng S (2023) Photoperiod and gravistimulation-associated Tiller Angle Control 1 modulates dynamic changes in rice plant architecture. Theor Appl Genetics 136:160. https://doi.org/10.1007/s00122-023-04404-z
Wu Y, Zhao S, Li X, Zhang B, Jiang L, Tang Y, Zhao J, Ma X, Cai H, Sun C, Tan L (2018) Deletions linked to PROG1 gene participate in plant architecture domestication in Asian and African rice. Nature Commun 9:1–10. https://doi.org/10.1038/s41467-018-06509-2
Xie C, Ge Z, An L, Chen X, Fang R (2019) Phytochrome-interacting factor-like protein OsPIL15 integrates light and gravitropism to regulate tiller angle in rice. Planta 250:105–114. https://doi.org/10.1007/s00425-019-03149-8
Xu D, Qi X, Li J, Han X, Wang J, Jiang Y, Tian Y, Wang Y (2017) PzTAC and PzLAZY from a narrow-crown poplar contribute to regulation of branch angles. Plant Physiol Biochem 118:571–578. https://doi.org/10.1016/j.plaphy.2017.07.011
Yan J, Zhu J, He C, Benmoussa M, Ping Wu (1999) Molecular marker-assisted dissection of genotype × environment interaction for plant type traits in rice (Oryza sativa L.). Crop Sci 39:538–544. https://doi.org/10.2135/cropsci1999.0011183X003900020039x
Yang P, Wen Q, Yu R, Chen H (2020) Light modulates the gravitropic responses through organ-specific PIFs and HY5 regulation of LAZY4 expression in Arabidopsis. Proc Natl Acad Sci USA 117:18840–18848. https://doi.org/10.1073/pnas.2005871117
Yoshihara T, 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. https://doi.org/10.1093/pcp/pcm042
Yoshihara T, Spalding EP (2017) LAZY genes mediate the effects of gravity on auxin gradients and plant architecture. Plant Physiol 175:959–969. https://doi.org/10.1104/pp.17.00942
Yu B, Lin Z, Li H, Li X, Li J, Wang Y, Zhang X, Zhu Z, Zhai W, Wang X, Xie D, Sun C (2007) TAC1, a major quantitative trait locus controlling tiller angle in rice. Plant J 52:891–898. https://doi.org/10.1111/j.1365-313x.2007.03284.x
Zhang N, Yu H, Cai Y, Huang L, Xu C, Xiong G, Meng X, Wang J, Chen H, Liu G, Jing Y, Yuan Y, Liang Y, Li S, Smith SM, Li J, Wang Y (2018) A core regulatory pathway controlling rice tiller angle mediated by the LAZY1-dependent asymmetric distribution of auxin. Plant Cell 30:1461–1475. https://doi.org/10.1105/tpc.18.00063
Zhang W, Tan L, Sun H, Zhao X, Liu F, Cai H, Fu Y, Sun X, Gu P, Zhu Z, Sun C (2019) Natural variations at TIG1 encoding a TCP transcription factor contribute to plant architecture domestication in rice. Mol Plant 12:1075–1089. https://doi.org/10.1016/j.molp.2019.04.005
Zhang H, Li X, Sang D, Huang L, Song Y, Du M, Cao J, Wang W (2022) PROG1 acts upstream of LAZY1 to regulate rice tiller angle as a repressor. Crop J 11:386–393. https://doi.org/10.1016/j.cj.2022.11.008
Zhao H, Hyai Z, Xiao Y, Wang X, Yu J, Ding G, Peng J (2014) Natural variation and genetic analysis of the tiller angle gene MsTAC1 in Miscanthus sinensis. Planta 240:161–175. https://doi.org/10.1007/s00425-014-2070-x
Zhao L, Zheng Y, Wang Y, Wang S, Wang C, Chen Y, Zhang K, Zhang N, Dong Z, Chen F (2023) A HST-like gene controls tiller angle through regulating endogenous auxin in common wheat. Plant Biotechnol J 21:122–135. https://doi.org/10.1111/pbi.13930
Acknowledgements
The authors thank Ms. S. Aoki, Ms. K. Iguchi, Mr. Y. Kotoku, Ms. Zin Mar Myint, Ms. S. Sasagawa, Ms. Y. Teraushi, and Mr. K. Yamaguchi for their technical assistance.
Funding
This work was supported by JSPS Grant-in-Aid for JSPS Fellows Grant Number 22J20329. Some of the rice accessions were provided by the National Institute of Genetics supported by the National Bioresource Project (NBRP), AMED, Japan. Computations were partially performed on the NIG supercomputer at ROIS National Institute of Genetics.
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YT and YKo: conceived the study; YT, MO, SK, KH, SO, and YKo: conducted the experiments; YT, MO, KO, and TI: produced genetic resources; YKi and YKo: supervised the study; YT, MO, and YKo: wrote the draft of the manuscript, and all the authors reviewed the manuscript.
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Tokuyama, Y., Omachi, M., Kushida, S. et al. Different contributions of PROG1 and TAC1 to the angular kinematics of the main culm and tillers of wild rice (Oryza rufipogon). Planta 259, 19 (2024). https://doi.org/10.1007/s00425-023-04300-2
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DOI: https://doi.org/10.1007/s00425-023-04300-2