Antagonistic Regulation of the Gibberellic Acid Response During Stem Growth in Rice

Overview

Journal Nature

Specialty Science

Date 2020 Jul 17

PMID 32669710

Citations 59

Authors

Keisuke Nagai

Yoshinao Mori

Shin Ishikawa

Tomoyuki Furuta

Rico Gamuyao

Yoko Niimi

Tokunori Hobo

Moyuri Fukuda

Mikiko Kojima

Yumiko Takebayashi

Atsushi Fukushima

Yasuyo Himuro

Masatomo Kobayashi

Wataru Ackley

Hiroshi Hisano

Kazuhiro Sato

Aya Yoshida

Jianzhong Wu

Hitoshi Sakakibara

Yutaka Sato

Hiroyuki Tsuji

Takashi Akagi

Motoyuki Ashikari

Affiliations

Soon will be listed here.

Abstract

The size of plants is largely determined by growth of the stem. Stem elongation is stimulated by gibberellic acid. Here we show that internode stem elongation in rice is regulated antagonistically by an 'accelerator' and a 'decelerator' in concert with gibberellic acid. Expression of a gene we name ACCELERATOR OF INTERNODE ELONGATION 1 (ACE1), which encodes a protein of unknown function, confers cells of the intercalary meristematic region with the competence for cell division, leading to internode elongation in the presence of gibberellic acid. By contrast, upregulation of DECELERATOR OF INTERNODE ELONGATION 1 (DEC1), which encodes a zinc-finger transcription factor, suppresses internode elongation, whereas downregulation of DEC1 allows internode elongation. We also show that the mechanism of internode elongation that is mediated by ACE1 and DEC1 is conserved in the Gramineae family. Furthermore, an analysis of genetic diversity suggests that mutations in ACE1 and DEC1 have historically contributed to the selection of shorter plants in domesticated populations of rice to increase their resistance to lodging, and of taller plants in wild species of rice for adaptation to growth in deep water. Our identification of these antagonistic regulatory factors enhances our understanding of the gibberellic acid response as an additional mechanism that regulates internode elongation and environmental fitness, beyond biosynthesis and gibberellic acid signal transduction.

Citing Articles

Identification of Submergence Tolerance Loci in Dongxiang Wild Rice (DXWR) by Genetic Linkage and Transcriptome Analyses.

Wang J, Huang C, Tang L, Chen H, Chen P, Chen D Int J Mol Sci. 2025; 26(5).

PMID: 40076455 PMC: 11898957. DOI: 10.3390/ijms26051829.

Subgenome asymmetry of gibberellins-related genes plays important roles in regulating rapid growth of bamboos.

Mao L, Guo C, Niu L, Wang Y, Jin G, Yang Y Plant Divers. 2025; 47(1):68-81.

PMID: 40041567 PMC: 11873579. DOI: 10.1016/j.pld.2024.10.004.

Detection of QTLs regulating the second internode length in rice dwarf mutant .

Ha Q, Moe S, Reyes V, Doi K, Miura K, Mizushima M Breed Sci. 2025; 74(5):443-453.

PMID: 39897668 PMC: 11780330. DOI: 10.1270/jsbbs.24036.

Surviving floods: Escape and quiescence strategies of rice coping with submergence.

Ashikari M, Nagai K, Bailey-Serres J Plant Physiol. 2025; 197(2).

PMID: 39880379 PMC: 11878773. DOI: 10.1093/plphys/kiaf029.

Elite Alleles of EPE1 Identified via Genome-wide Association Studies Increase Panicle Elongation Length in Rice.

Sun H, Yao Q, Hai M, Li T, Sun J, Liu Z Rice (N Y). 2025; 18(1):4.

PMID: 39878928 PMC: 11780047. DOI: 10.1186/s12284-025-00759-7.

References

Kaneko M, Itoh H, Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Ashikari M . Where do gibberellin biosynthesis and gibberellin signaling occur in rice plants?. Plant J. 2003; 35(1):104-15. DOI: 10.1046/j.1365-313x.2003.01780.x. View

Kende , van der Knaap E , CHO . Deepwater rice: A model plant to study stem elongation . Plant Physiol. 1998; 118(4):1105-10. PMC: 1539197. DOI: 10.1104/pp.118.4.1105. View

Sauter M, Mekhedov S, Kende H . Gibberellin promotes histone H1 kinase activity and the expression of cdc2 and cyclin genes during the induction of rapid growth in deepwater rice internodes. Plant J. 1995; 7(4):623-32. DOI: 10.1046/j.1365-313x.1995.7040623.x. View

Sasaki A, ASHIKARI M, Itoh H, Nishimura A, Swapan D, Ishiyama K . Green revolution: a mutant gibberellin-synthesis gene in rice. Nature. 2002; 416(6882):701-2. DOI: 10.1038/416701a. View

Peng J, RICHARDS D, Hartley N, Murphy G, Devos K, Flintham J . 'Green revolution' genes encode mutant gibberellin response modulators. Nature. 1999; 400(6741):256-61. DOI: 10.1038/22307. View

Kuroha T, Nagai K, Gamuyao R, Wang D, Furuta T, Nakamori M . Ethylene-gibberellin signaling underlies adaptation of rice to periodic flooding. Science. 2018; 361(6398):181-186. DOI: 10.1126/science.aat1577. View

Nagai K, Kondo Y, Kitaoka T, Noda T, Kuroha T, Angeles-Shim R . QTL analysis of internode elongation in response to gibberellin in deepwater rice. AoB Plants. 2014; 6. PMC: 4086424. DOI: 10.1093/aobpla/plu028. View

Kotogany E, Dudits D, Horvath G, Ayaydin F . A rapid and robust assay for detection of S-phase cell cycle progression in plant cells and tissues by using ethynyl deoxyuridine. Plant Methods. 2010; 6(1):5. PMC: 2828981. DOI: 10.1186/1746-4811-6-5. View

Kania T, Russenberger D, Peng S, Apel K, Melzer S . FPF1 promotes flowering in Arabidopsis. Plant Cell. 1997; 9(8):1327-38. PMC: 157001. DOI: 10.1105/tpc.9.8.1327. View

10.

Sakamoto T, Miura K, Itoh H, Tatsumi T, Ueguchi-Tanaka M, Ishiyama K . An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiol. 2004; 134(4):1642-53. PMC: 419838. DOI: 10.1104/pp.103.033696. View

11.

Hattori Y, Nagai K, Furukawa S, Song X, Kawano R, Sakakibara H . The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature. 2009; 460(7258):1026-30. DOI: 10.1038/nature08258. View

12.

Gomez-Ariza J, Brambilla V, Vicentini G, Landini M, Cerise M, Carrera E . A transcription factor coordinating internode elongation and photoperiodic signals in rice. Nat Plants. 2019; 5(4):358-362. DOI: 10.1038/s41477-019-0401-4. View

13.

Pauwels L, Barbero G, Geerinck J, Tilleman S, Grunewald W, Cuellar Perez A . NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature. 2010; 464(7289):788-91. PMC: 2849182. DOI: 10.1038/nature08854. View

14.

Li S, Zhao B, Yuan D, Duan M, Qian Q, Tang L . Rice zinc finger protein DST enhances grain production through controlling Gn1a/OsCKX2 expression. Proc Natl Acad Sci U S A. 2013; 110(8):3167-72. PMC: 3581943. DOI: 10.1073/pnas.1300359110. View

15.

Kojima M, Kamada-Nobusada T, Komatsu H, Takei K, Kuroha T, Mizutani M . Highly sensitive and high-throughput analysis of plant hormones using MS-probe modification and liquid chromatography-tandem mass spectrometry: an application for hormone profiling in Oryza sativa. Plant Cell Physiol. 2009; 50(7):1201-14. PMC: 2709547. DOI: 10.1093/pcp/pcp057. View

16.

Shinozaki Y, Hao S, Kojima M, Sakakibara H, Ozeki-Iida Y, Zheng Y . Ethylene suppresses tomato (Solanum lycopersicum) fruit set through modification of gibberellin metabolism. Plant J. 2015; 83(2):237-51. DOI: 10.1111/tpj.12882. View

17.

Minami A, Nagao M, Ikegami K, Koshiba T, Arakawa K, Fujikawa S . Cold acclimation in bryophytes: low-temperature-induced freezing tolerance in Physcomitrella patens is associated with increases in expression levels of stress-related genes but not with increase in level of endogenous abscisic acid. Planta. 2004; 220(3):414-23. DOI: 10.1007/s00425-004-1361-z. View

18.

Ueguchi-Tanaka M, Nakajima M, Katoh E, Ohmiya H, Asano K, Saji S . Molecular interactions of a soluble gibberellin receptor, GID1, with a rice DELLA protein, SLR1, and gibberellin. Plant Cell. 2007; 19(7):2140-55. PMC: 1955699. DOI: 10.1105/tpc.106.043729. View

19.

Mikami M, Toki S, Endo M . Comparison of CRISPR/Cas9 expression constructs for efficient targeted mutagenesis in rice. Plant Mol Biol. 2015; 88(6):561-72. PMC: 4523696. DOI: 10.1007/s11103-015-0342-x. View

20.

Hiei Y, Ohta S, Komari T, Kumashiro T . Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 1994; 6(2):271-82. DOI: 10.1046/j.1365-313x.1994.6020271.x. View