Overexpression of rice gene OsATG8b confers tolerance to nitrogen starvation and increases yield and nitrogen use efficiency (NUE) in Arabidopsis
Autoři:
Xiaoxi Zhen aff001; Fan Xu aff001; Wenzhong Zhang aff001; Nan Li aff002; Xin Li aff001
Působiště autorů:
Rice Research Institute of Shenyang Agricultural University, Key Laboratory of Northern Japonica Rice Genetics and Breeding, Ministry of Education and Liaoning Province, Key Laboratory of Northeast Rice Biology and Genetics and Breeding, Ministry of Agric
aff001; Shen Yang Product Quality Supervision and Inspection Institute, Shenyang, China
aff002
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0223011
Souhrn
Nitrogen (N) is an important element required for plant growth and development, which also affects plant yield and quality. Autophagy, a conserved pathway in eukaryotes, degrades and recycles cellular components, thus playing an important role in N remobilization. However, only a few autophagy genes related to N remobilization in rice (Oryza sativa) have been reported. Here, we identified a core autophagy gene in rice, OsATG8b, with increased expression levels under N starvation conditions. It was investigated the function of OsATG8b by generating three independent homozygous 35S-OsATG8b transgenic Arabidopsis thaliana lines. The overexpression of OsATG8b significantly enhanced autophagic flux in the transgenic Arabidopsis plants. It was also showed that over-expressing OsATG8b promoted growth and development of Arabidopsis, in which the rosette leaves were larger than those of the wild type (WT), and the yield increased significantly by 25.25%. In addition, the transgenic lines accumulated more N in seeds than in the rosette leaves. Further examination revealed that overexpression of OsATG8b could effectively alleviate the growth inhibition of transgenic Arabidopsis under nitrogen (N) stress. N partitioning studies revealed that nitrogen-harvest index (NHI) and nitrogen use efficiency (NUE) were significantly increased in the transgenic Arabidopsis, as well as the 15N-tracer experiments revealing that the remobilization of N to seeds in the OsATG8b-overexpressing transgenic Arabidopsis was high and more than WT. Based on our findings, we consider OsATG8b to be a great candidate gene to increase NUE and yield, especially under suboptimal field conditions.
Klíčová slova:
Rice – Hyperexpression techniques – Autophagic cell death – Genetically modified plants – Leaves – Seeds – Seedlings – Arabidopsis thaliana
Zdroje
1. Kraiser T, Gras DE, Gutiérrez AG, González B, Gutiérrez RA. A holistic view of nitrogen acquisition in plants. Journal of Experimental Botany. 2011; 62: 1455–1466. doi: 10.1093/jxb/erq425 21239377
2. Havé M, Balliau T, Cottyn-Boitte B, Dérond E, Cueff G, Soulay F, et al. Increase of proteasome and papain-like cysteine protease activities in autophagy mutants: backup compensatory effect or pro cell-death effect? Journal of Experimental Botany. 2017; 69: 1369–1385.
3. Chardon F, Noël V, Masclaux-Daubresse C. Exploring NUE in crops and in Arabidopsis ideotypes to improve yield and seed quality. Journal of Experimental Botany. 2012; 63: 3401–3412. doi: 10.1093/jxb/err353 22231501
4. Avila-Ospina L, Masclaux-Daubresse C. Autophagy, plant senescence, and nutrient recycling. Journal of Experimental Botany. 2014; 65: 3799–3811. doi: 10.1093/jxb/eru039 24687977
5. Krapp A. Plant nitrogen assimilation and its regulation: a complex puzzle with missing pieces. Current Opinion in Plant Biology. 2015; 25: 115–122. doi: 10.1016/j.pbi.2015.05.010 26037390
6. Makino A, Osmond B. Effects of Nitrogen Nutrition on Nitrogen Partitioning between Chloroplasts and Mitochondria in Pea and Wheat. Plant Physiology. 1991; 96: 355–362. doi: 10.1104/pp.96.2.355 16668193
7. Masclaux-Daubresse C, Daniel-Vedele F, Dechorgnat J, Chardon F, Gaufichon L, Suzuki A, et al. Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Annals of Botany. 2010; 105: 1141–1157. doi: 10.1093/aob/mcq028 20299346
8. Masclaux-Daubresse C, Chardon F. Exploring nitrogen remobilization for seed filling using natural variation in Arabidopsis thaliana. Journal of Experimental Botany. 2011; 62: 2131–2142. doi: 10.1093/jxb/erq405 21273332
9. Patrick JW, Offler CE. Compartmentation of transport and transfer events in developing seeds. Journal of Experimental Botany. 2001; 52: 551–564. 11373304
10. Roberts IN, Caputo C, Criado MV, Funk C. Senescence-associated proteases in plants. Physiologia Plantarum. 2012; 145: 130–139. doi: 10.1111/j.1399-3054.2012.01574.x 22242903
11. Marshall RS, Vierstra RD. Autophagy: The Master of Bulk and Selective Recycling. Annual Review of Plant Biology. 2018; 69: 173–208. doi: 10.1146/annurev-arplant-042817-040606 29539270
12. Yang X, Bassham DC. New Insight into the Mechanism and Function of Autophagy in Plant Cells. International Review of Cell & Molecular Biology. 2015; 320: 1–40.
13. Tsukada M, Ohsumi Y. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. Febs Letters. 1993; 333: 169–174. doi: 10.1016/0014-5793(93)80398-e 8224160
14. Feng Y, He D, Yao Z, Klionsky DJ. The machinery of macroautophagy. Cell Research. 2014; 24: 24–41. doi: 10.1038/cr.2013.168 24366339
15. Yao Z, Delorme-Axford E, Backues SK, Klionsky DJ. Atg41/Icy2 regulates autophagosome formation. Autophagy. 2015; 11: 2288–2299. doi: 10.1080/15548627.2015.1107692 26565778
16. Rose TL, Bonneau L, Der C, Marty-Mazars D, Marty F. Starvation-induced expression of autophagy-related genes in Arabidopsis. Biology of the Cell. 2006; 98: 53–67. doi: 10.1042/BC20040516 16354162
17. Thomas H. Senescence, ageing and death of the whole plant. New Phytologist. 2012; 197: 696–711. doi: 10.1111/nph.12047 23176101
18. Liu Y, Bassham DC. Autophagy: pathways for self-eating in plant cells. Annual Review of Plant Biology. 2012; 63: 215–237. doi: 10.1146/annurev-arplant-042811-105441 22242963
19. Yoshimoto K, Jikumaru Y, Kamiya Y, Kusano M, Consonni C, Panstruga R, et al. Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell. 2009; 21: 2914–2927. doi: 10.1105/tpc.109.068635 19773385
20. Guiboileau A, Yoshimoto K, Soulay F, Bataillé MP, Avice JC, Masclaux-Daubresse C, et al. Autophagy machinery controls nitrogen remobilization at the whole-plant level under both limiting and ample nitrate conditions in Arabidopsis. New Phytologist. 2012; 194: 732–740. doi: 10.1111/j.1469-8137.2012.04084.x 22404536
21. Wada S, Hayashida Y, Izumi M, Kurusu T, Hanamata S, Kanno K. Autophagy supports biomass production and nitrogen use efficiency at the vegetative stage in rice. Plant Physiology. 2015; 168: 60–73. doi: 10.1104/pp.15.00242 25786829
22. Li F, Chung T, Pennington JG, Federico ML, Kaeppler HF, Kaeppler SM, et al. Autophagic recycling plays a central role in maize nitrogen remobilization. Plant Cell. 2015; 27: 1389–1408. doi: 10.1105/tpc.15.00158 25944100
23. Xie Z, Nair U, Klionsky DJ. An InCytes from MBC Selection: Atg8 Controls Phagophore Expansion during Autophagosome Formation. Molecular Biology of the Cell. 2008; 19: 3290. doi: 10.1091/mbc.E07-12-1292 18508918
24. Masclaux-Daubresse C, Chen Q, Havé M. Regulation of nutrient recycling via autophagy. Current Opinion in Plant Biology. 2017; 39: 8–17. doi: 10.1016/j.pbi.2017.05.001 28528166
25. Kellner R, De la Concepcion JC, Maqbool A, Kamoun S, Dagdas YF. ATG8 Expansion: A Driver of Selective Autophagy Diversification? Trends in Plant Science. 2016; 22: 204–214. doi: 10.1016/j.tplants.2016.11.015 28038982
26. Avin-Wittenberg T, Honig A, Galili G. Variations on a theme: plant autophagy in comparison to yeast and mammals. Protoplasma. 2012; 249: 285–299. doi: 10.1007/s00709-011-0296-z 21660427
27. Su W, Ma H, Liu C, Wu J, Yang J. Identification and characterization of two rice autophagy associated genes, OsAtg8 and OsAtg4. Molecular biology reports. 2006; 33: 273–278. doi: 10.1007/s11033-006-9011-0 17082902
28. Chung T, Suttangkakul A, Vierstra RD. The ATG autophagic conjugation system in maize: ATG transcripts and abundance of the ATG8-lipid adduct are regulated by development and nutrient availability. Plant Physiology. 2009; 149: 220–234. doi: 10.1104/pp.108.126714 18790996
29. Xia K, Liu T, Ouyang J, Wang R, Fan T, Zhang M. Genome-Wide Identification, Classification, and Expression Analysis of Autophagy-Associated Gene Homologues in Rice (Oryza sativa L.). DNA Research. 2011; 18: 363–377. doi: 10.1093/dnares/dsr024 21795261
30. Xia T, Xiao D, Liu D, Chai W, Gong Q, Wang N. Heterologous expression of ATG8c from soybean confers tolerance to nitrogen deficiency and increases yield in Arabidopsis. PLoS ONE. 2012; 7: e37217. doi: 10.1371/journal.pone.0037217 22629371
31. Slavikova S, Ufaz S, Avin-Wittenberg T, Levanony H, Galili G. An autophagy-associated Atg8 protein is involved in the responses of Arabidopsis seedlings to hormonal controls and abiotic stresses. Journal of Experimental Botany. 2008; 59: 4029–4043. doi: 10.1093/jxb/ern244 18836138
32. Wang P, Sun X, Jia X, Wang N, Gong X, Ma F. Characterization of an autophagy-related gene MdATG8i from apple. Frontiers in plant science. 2016; 7: 720. doi: 10.3389/fpls.2016.00720 27252732
33. Li W, Chen M, Zhong L, Liu JM, Xu ZS, Li L, et al. Overexpression of the autophagy-related gene SiATG8a from foxtail millet (Setaria italica L.) confers tolerance to both nitrogen starvation and drought stress in Arabidopsis. Biochemical & Biophysical Research Communications. 2015; 468: 800–806.
34. Li W, Chen M, Wang E, Hu L, Hawkesford MJ, Zhong L, et al. Genome-wide analysis of autophagy-associated genes in foxtail millet (Setaria italica L.) and characterization of the function of SiATG8a in conferring tolerance to nitrogen starvation in rice. BMC Genomics. 2016; 17: 797. doi: 10.1186/s12864-016-3113-4 27733118
35. Chen Q, Soulay F, Saudemont B, Elmayan T, Marmagne A, Masclaux-Daubresse C. Overexpression of ATG8 in Arabidopsis stimulates autophagic activity and increases nitrogen remobilization efficiency and grain filling. Plant and Cell Physiology. 2019; 60: 343–352. doi: 10.1093/pcp/pcy214 30407574
36. Ishida H, Yoshimoto K, Izumi M, Reisen D, Yano Y, Noda T, et al. Mobilization of rubisco and stroma-localized fluorescent proteins of chloroplasts to the vacuole by an ATG gene-dependent autophagic process. Plant Physiology. 2008; 148: 142–155. doi: 10.1104/pp.108.122770 18614709
37. Yoshimoto K, Hanaoka H, Sato S, Kato T, Tabata S, Noda T, et al. Processing of ATG8s, Ubiquitin-Like Proteins, and Their Deconjugation by ATG4s Are Essential for Plant Autophagy. Plant Cell. 2004; 16: 2967–2983. doi: 10.1105/tpc.104.025395 15494556
38. Hafrén A, Macia JL, Love AJ, Milner JJ, Drucker M, Hofius D. Selective autophagy limits cauliflower mosaic virus infection by NBR1-mediated targeting of viral capsid protein and particles. Proceedings of the National Academy of Sciences. 2017; 114: E2026–E2035.
39. Svenning S, Lamark T, Krause K, Johansen T. Plant NBR1 is a selective autophagy substrate and a functional hybrid of the mammalian autophagic adapters NBR1 and p62/SQSTM1. Autophagy. 2011; 7: 993–1010. doi: 10.4161/auto.7.9.16389 21606687
40. Klionsky DJ, Schulman BA. Dynamic regulation of macroautophagy by distinctive ubiquitin-like proteins. Nature structural & molecular biology. 2014; 21: 336–345.
41. Zhu T, Zou L, Li Y, Yao X, Xu F, Deng X, et al. Mitochondrial alternative oxidase-dependent autophagy involved in ethylene-mediated drought tolerance in Solanum lycopersicum. Plant Biotechnology Journal. 2018; 16: 2063–2076. doi: 10.1111/pbi.12939 29729068
42. Contento AL, Xiong Y, Bassham DC. Visualization of autophagy in Arabidopsis using the fluorescent dye monodansylcadaverine and a GFP‐AtATG8e fusion protein. The Plant Journal. 2005; 42: 598–608. doi: 10.1111/j.1365-313X.2005.02396.x 15860017
43. Seglen PO, Gordon PB. 3-Methyladenine: Specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proceedings of the National Academy of Sciences of the United States of America. 1982; 79: 1889–1892. doi: 10.1073/pnas.79.6.1889 6952238
44. Inoue Y, Suzuki T, Hattori M, Yoshimoto K, Ohsumi Y, Moriyasu Y. AtATG genes, homologs of yeast autophagy genes, are involved in constitutive autophagy in Arabidopsis root tip cells. Plant & Cell Physiology. 2006; 47: 1641–1652.
45. Moriyasu Y, Ohsumi Y. Autophagy in tobacco suspension-cultured cells in response to sucrose starvation. Plant Physiology. 1996; 111: 1233–1241. doi: 10.1104/pp.111.4.1233 12226358
46. Thompson AR, Doelling JH, Suttangkakul A, Vierstra RD. Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiology. 2005; 138: 2097–2110. doi: 10.1104/pp.105.060673 16040659
47. Sun X, Jia X, Huo L, Che R, Gong X, Wang P, et al. MdATG18a overexpression improves tolerance to nitrogen deficiency and regulates anthocyanin accumulation through increased autophagy in transgenic apple. Plant Cell & Environment. 2018; 41: 469–480.
48. Wang Y, Yu B, Zhao J, Guo J, Li Y, Han S, et al. Autophagy contributes to leaf starch degradation. Plant Cell. 2013; 25: 1383–1399. doi: 10.1105/tpc.112.108993 23564204
49. Barros JA, Cavalcanti JHF, Medeiros DB, Nunes-Nesi A, Avin-Wittenberg T, Fernie AR, et al. Autophagy deficiency compromises alternative pathways of respiration following energy deprivation. Plant Physiology. 2017; 175: 62–76. doi: 10.1104/pp.16.01576 28710132
50. Ren C, Liu J, Gong Q. Functions of autophagy in plant carbon and nitrogen metabolism. Frontiers in plant science. 2014; 5: 301. doi: 10.3389/fpls.2014.00301 25009547
51. Liu D, Gong QQ, Ma YY, Li PL, Li JP, Yang SH, et al. cpSecA, a thylakoid protein translocase subunit, is essential for photosynthetic development in Arabidopsis. Journal of Experimental Botany. 2010; 61: 1655–1669. doi: 10.1093/jxb/erq033 20194926
52. Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium‐mediated transformation of Arabidopsis thaliana. The Plant Journal. 1998; 16: 735–743. doi: 10.1046/j.1365-313x.1998.00343.x 10069079
53. Boyes DC, Zayed AM, Ascenzi R, Mccaskill AJ, Hoffman NE, Davis KR, et al. Growth Stage-Based Phenotypic Analysis of Arabidopsis: A Model for High Throughput Functional Genomics in Plants. Plant Cell. 2001; 13: 1499–1510. doi: 10.1105/TPC.010011 11449047
54. Xu F, Meng T, Li P, Yu Y, Cui Y, Wang Y, et al. A Soybean Dual-Specificity Kinase, GmSARK, and Its Arabidopsis Homolog, AtSARK, Regulate Leaf Senescence through Synergistic Actions of Auxin and Ethylene. Plant Physiology. 2011; 157: 2131–2153. doi: 10.1104/pp.111.182899 22034630
55. Arnon DI. Copper Enzymes in Isolated Chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology. 1949; 24: 1–15. doi: 10.1104/pp.24.1.1 16654194
56. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry. 1976; 72: 248–254. doi: 10.1006/abio.1976.9999 942051
57. Ferrario-Méry S, Valadier MH, Foyer CH. Overexpression of nitrate reductase in tobacco delays drought-induced decreases in nitrate reductase activity and mRNA. Plant Physiology. 1998; 117: 293–302. doi: 10.1104/pp.117.1.293 9576799
Článok vyšiel v časopise
PLOS One
2019 Číslo 9
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Úspěšná resuscitativní thorakotomie v přednemocniční neodkladné péči
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Graviola (Annona muricata) attenuates behavioural alterations and testicular oxidative stress induced by streptozotocin in diabetic rats
- CH(II), a cerebroprotein hydrolysate, exhibits potential neuro-protective effect on Alzheimer’s disease
- Comparison between Aptima Assays (Hologic) and the Allplex STI Essential Assay (Seegene) for the diagnosis of Sexually transmitted infections
- Assessment of glucose-6-phosphate dehydrogenase activity using CareStart G6PD rapid diagnostic test and associated genetic variants in Plasmodium vivax malaria endemic setting in Mauritania