Histone Acetyltransferase GCN5 Regulates Rice Growth and Development and Enhances Salt Tolerance
Received date: 2024-03-03
Accepted date: 2024-06-03
Online published: 2024-12-10
Histone acetylation is indispensable in the process of crops resisting abiotic stress, which is jointly catalyzed by histone acetyltransferases and deacetylases. However, the mechanism of regulating salt tolerance through histone acetyltransferase GCN5 is still unclear. We revealed that GCN5 can catalyze the acetylation of canonical H3 and H4 lysine residues both in vivo and in vitro in rice. The knockout mutants and RNA interference lines of OsGCN5 exhibited severe growth inhibition and defects in salt tolerance, while the over-expression of OsGCN5 enhanced the salt tolerance of rice seedlings, indicating that OsGCN5 positively regulated the response of rice to salt stress. RNA-seq analysis suggested OsGCN5 may positively regulate the salt tolerance of rice by inhibiting the expression of OsHKT2;1 or other salt-responsive genes. Taken together, our study indicated that GCN5 plays a key role in enhancing salt tolerance in rice.
Key words： GCN5; histone acetyltransferase; salt tolerance; Oryza sativa
Xue Chao, Zhao Xinru, Chen Xu, Cai Xingjing, Hu Yingying, Li Xiya, Zhou Yong, Gong Zhiyun . Histone Acetyltransferase GCN5 Regulates Rice Growth and Development and Enhances Salt Tolerance[J]. Rice Science, 2024 , 31(6) : 688 -699 . DOI: 10.1016/j.rsci.2024.06.002
| [1] | An D, Chen J G, Gao Y Q, Li X, Chao Z F, Chen Z R, Li Q Q, Han M L, Wang Y L, Wang Y F, Chao D Y. 2017. AtHKT1 drives adaptation of Arabidopsis thaliana to salinity by reducing floral sodium content. PLoS Genet, 13(10): e1007086. |
| [2] | Ardie S W, Xie L N, Takahashi R, Liu S K, Takano T. 2009. Cloning of a high-affinity K+ transporter gene PutHKT2;1 from Puccinellia tenuiflora and its functional comparison with OsHKT2;1 from rice in yeast and Arabidopsis. J Exp Bot, 60(12): 3491-3502. |
| [3] | Grant P A, Duggan L, Côté J, Roberts S M, Brownell J E, Candau R, Ohba R, Owen-Hughes T, Allis C D, Winston F, Berger S L, Workman J L. 1997. Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: Characterization of an Ada complex and the SAGA (Spt/Ada) complex. Genes Dev, 11(13): 1640-1650. |
| [4] | Hawar A, Xiong S Q, Yang Z, Sun B. 2022. Histone acetyltransferase SlGCN5 regulates shoot meristem and flower development in Solanum lycopersicum. Front Plant Sci, 12: 805879. |
| [5] | Horie T, Costa A, Kim T H, Han M J, Horie R, Leung H Y, Miyao A, Hirochika H, An G, Schroeder J I. 2007. Rice OsHKT2;1 transporter mediates large Na+ influx component into K+-starved roots for growth. EMBO J, 26(12): 3003-3014. |
| [6] | Hu J Z, Cai J, Park S J, Lee K, Li Y X, Chen Y, Yun J Y, Xu T, Kang H. 2021. N6-Methyladenosine mRNA methylation is important for salt stress tolerance in Arabidopsis. Plant J, 106(6): 1759-1775. |
| [7] | Hu Z R, Song N, Zheng M, Liu X Y, Liu Z S, Xing J W, Ma J H, Guo W W, Yao Y Y, Peng H R, Xin M M, Zhou D X, Ni Z F, Sun Q X. 2015. Histone acetyltransferase GCN5 is essential for heat stress-responsive gene activation and thermotolerance in Arabidopsis. Plant J, 84(6): 1178-1191. |
| [8] | Jha U C, Chaturvedi S K, Bohra A, Basu P S, Khan M S, Barh D. 2014. Abiotic stresses, constraints and improvement strategies in chickpea. Plant Breed, 133(2): 163-178. |
| [9] | Kim S, Piquerez S J M, Ramirez-Prado J S, Mastorakis E, Veluchamy A, Latrasse D, Manza-Mianza D, Brik-Chaouche R, Huang Y, Rodriguez- Granados N Y, Concia L, Blein T, Citerne S, Bendahmane A, Bergounioux C, Crespi M, Mahfouz M M, Raynaud C, Hirt H, Ntoukakis V, Benhamed M. 2020. GCN5 modulates salicylic acid homeostasis by regulating H3K14ac levels at the 5′ and 3′ ends of its target genes. Nucleic Acids Res, 48(11): 5953-5966. |
| [10] | Kobayashi N I, Yamaji N, Yamamoto H, Okubo K, Ueno H, Costa A, Tanoi K, Matsumura H, Fujii-Kashino M, Horiuchi T, Nayef M A, Shabala S, An G, Ma J F, Horie T. 2017. OsHKT1;5 mediates Na+ exclusion in the vasculature to protect leaf blades and reproductive tissues from salt toxicity in rice. Plant J, 91(4): 657-670. |
| [11] | Kotak J, Saisana M, Gegas V, Pechlivani N, Kaldis A, Papoutsoglou P, Makris A, Burns J, Kendig A L, Sheikh M, Kuschner C E, Whitney G, Caiola H, Doonan J H, Vlachonasios K E, McCain E R, Hark A T. 2018. The histone acetyltransferase GCN5 and the transcriptional coactivator ADA2b affect leaf development and trichome morphogenesis in Arabidopsis. Planta, 248(3): 613-628. |
| [12] | Kubo T, Yoshimura A, Kurata N. 2022. Loss of OsEAF6, a subunit of the histone acetyltransferase complex, causes hybrid breakdown in intersubspecific rice crosses. Front Plant Sci, 13: 866404. |
| [13] | Kumar V, Thakur J K, Prasad M. 2021. Histone acetylation dynamics regulating plant development and stress responses. Cell Mol Life Sci, 78(10): 4467-4486. |
| [14] | Li H, Yan S H, Zhao L, Tan J J, Zhang Q, Gao F, Wang P, Hou H L, Li L J. 2014. Histone acetylation associated up-regulation of the cell wall related genes is involved in salt stress induced maize root swelling. BMC Plant Biol, 14: 105. |
| [15] | Li S, Lin Y C J, Wang P Y, Zhang B F, Li M, Chen S, Shi R, Tunlaya-Anukit S, Liu X Y, Wang Z F, Dai X F, Yu J, Zhou C G, Liu B G, Wang J P, Chiang V L, Li W. 2019. transcription factor influences histone acetylation to regulate drought responses and tolerance in Populus trichocarpa. Plant Cell, 31(3): 663-686. |
| [16] | Li Z, Zhang H, Cai C J, Lin Z, Zhen Z, Chu J, Guo K. 2022. Histone acetyltransferase GCN5-mediated lysine acetylation modulates salt stress aadaption of Trichoderma. Appl Microbiol Biotechnol, 106(8): 3033-3049. |
| [17] | Liao B, Xiang Y H, Li Y, Yang K Y, Shan J X, Ye W W, Dong N Q, Kan Y, Yang Y B, Zhao H Y, Yu H X, Lu Z Q, Zhao Y, Zhao Q, Guo D L, Guo S Q, Lei J J, Mu X R, Cao Y J, Han B, Lin H X. 2024. Dysfunction of duplicated pair rice histone acetyltransferases causes segregation distortion and an interspecific reproductive barrier. Nat Commun, 15(1): 996. |
| [18] | Lin C J, Yang S Y, Hsu L H, Yu S J, Chen Y L. 2023. The Gcn5- Ada2-Ada3 histone acetyltransferase module has divergent roles in pathogenesis of Candida glabrata. Med Mycol, 61( 2): myad004. |
| [19] | Oomen R J F J, Benito B, Sentenac H, Rodríguez-Navarro A, Talón M, Véry A A, Domingo C. 2012. HKT2;2/1, a K?-permeable transporter identified in a salt-tolerant rice cultivar through surveys of natural genetic polymorphism. Plant J, 71(5): 750-762. |
| [20] | Poulios S, Tsilimigka F, Mallioura A, Pappas D, Seira E, Vlachonasios K. 2022. Histone acetyltransferase GCN5 affects auxin transport during root growth by modulating histone acetylation and gene expression of PINs. Plants, 11(24): 3572. |
| [21] | Roodt D. 2021. Worth its salt: A histone acetyltransferase gene enhances salt tolerance in bread wheat. Plant Physiol, 186(4): 1752-1753. |
| [22] | Servet C, Conde e S N, Zhou D X. 2010. Histone acetyltransferase AtGCN5/HAG1 is a versatile regulator of developmental and inducible gene expression in Arabidopsis. Molecular Plant. 3(4): 670-677. |
| [23] | Suzuki K, Yamaji N, Costa A, Okuma E, Kobayashi N I, Kashiwagi T, Katsuhara M, Wang C, Tanoi K, Murata Y, Schroeder J I, Ma J F, Horie T. 2016. OsHKT1;4-mediated Na+ transport in stems contributes to Na+ exclusion from leaf blades of rice at the reproductive growth stage upon salt stress. BMC Plant Biol, 16: 22. |
| [24] | Wang H, Jiao X, Kong X, Hamera S, Wu Y, Chen X, Fang R, Yan Y. 2016. A signaling cascade from miR444 to RDR1 in rice antiviral RNA silencing pathway. Plant Physiol, 170(4): 2365-2377. |
| [25] | Wang L, Dent S Y R. 2014. Functions of SAGA in development and disease. Epigenomics, 6(3): 329-339. |
| [26] | Wang R, Jing W, Xiao L Y, Jin Y K, Shen L K, Zhang W H. 2015. The rice high-affinity potassium Transporter1;1 is involved in salt tolerance and regulated by an MYB-type transcription factor. Plant Physiol, 168(3): 1076-1090. |
| [27] | Wang W X, Vinocur B, Altman A. 2003. Plant responses to drought, salinity and extreme temperatures: Towards genetic engineering for stress tolerance. Planta, 218(1): 1-14. |
| [28] | Weake V M, Workman J L. 2012. SAGA function in tissue-specific gene expression. Trends Cell Biol, 22(4): 177-184. |
| [29] | Wei H, Wang X L, He Y Q, Xu H, Wang L. 2021. Clock component OsPRR73 positively regulates rice salt tolerance by modulating OsHKT2;1-mediated sodium homeostasis. EMBO J, 40(3): e105086. |
| [30] | Wu C J, Yuan D Y, Liu Z Z, Xu X, Wei L, Cai X W, Su Y N, Li L, Chen S, He X J. 2023. Conserved and plant-specific histone acetyltransferase complexes cooperate to regulate gene transcription and plant development. Nat Plants, 9(3): 442-459. |
| [31] | Xue C, Liu S, Chen C, Zhu J., Yang X B, Zhou Y, Guo R, Liu X Y, Gong Z Y. 2018. Global proteome analysis links lysine acetylation to diverse functions in Oryza Sativa. Proteomics, 18(1): doi: 10.1002/pmic.201700036. |
| [32] | Yang Y Q, Guo Y. 2018. Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytol, 217(2): 523-539. |
| [33] | Zhang M X, Zhao R R, Wang H T, Ren S L, Shi L Y, Huang S Z, Wei Z Q, Guo B Y, Jin J Y, Zhong Y, Chen M J, Jiang W Z, Wu T, Du X L. 2023. OsWRKY28 positively regulates salinity tolerance by directly activating OsDREB1B expression in rice. Plant Cell Rep, 42(2): 223-234. |
| [34] | Zhao S, Zhang X R, Li H T. 2018. Beyond histone acetylation-writing and erasing histone acylations. Curr Opin Struct Biol, 53: 169-177. |
| [35] | Zheng M, Liu X B, Lin J C, Liu X Y, Wang Z Y, Xin M M, Yao Y Y, Peng H R, Zhou D X, Ni Z F, Sun Q X, Hu Z R. 2019. Histone acetyltransferase GCN5 contributes to cell wall integrity and salt stress tolerance by altering the expression of cellulose synthesis genes. Plant J, 97(3): 587-602. |
| [36] | Zheng M, Lin J C, Liu X B, Chu W, Li J P, Gao Y J, An K X, Song W J, Xin M M, Yao Y Y, Peng H R, Ni Z F, Sun Q X, Hu Z R. 2021. Histone acetyltransferase TaHAG1 acts as a crucial regulator to strengthen salt tolerance of hexaploid wheat. Plant Physiol, 186(4): 1951-1969. |
| [37] | Zhou S L, Jiang W, Long F, Cheng S F, Yang W J, Zhao Y, Zhou D X. 2017. Rice homeodomain protein WOX11 recruits a histone acetyltransferase complex to establish programs of cell proliferation of crown root meristem. Plant Cell, 29(5): 1088-1104. |
| [38] | Zhu J K. 2016. Abiotic stress signaling and responses in plants. Cell, 167(2): 313-324. |
/
| 〈 |
|
〉 |