AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home The Crop Journal Article
PDF (2.8 MB)
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research paper | Open Access

ALM1, encoding a Fe-superoxide dismutase, is critical for rice chloroplast biogenesis and drought stress response

Yanwei Wanga,1, Chen Denga,1, Pengfei Aib, Xue'an Cuia( ), Zhiguo Zhanga( )
Joint CAAS/IRRI Laboratory for Photosynthetic Enhancement, Biotechnology Research Institute/National Key Facility for Genetic Resources and Gene Improvement, Chinese Academy of Agricultural Sciences, Beijing 100081, China
College of Bioscience and Bioengineering, Hebei University of Science and Technology, Shijiazhuang 050000, Hebei, China

1 These authors contributed equally to this work.

Show Author Information

Abstract

Chloroplasts are the center of plant life activities including photosynthesis, growth and development, and abiotic stress response. Chloroplast development and biogenesis in rice have been studied in detail, but how does abiotic stress affect chloroplasts is less studied. We obtained an albino mutant, alm1, whose chlorophyll content was greatly decreased. Transmission electron microscopy showed that chloroplast development in alm1 was blocked, especially in thylakoid-like structures, which could not form normally. The ALM1 gene encodes a chloroplast-localized superoxide dismutase. Full-length ALM1 successfully restored the non-albino phenotype, and in knockout lines, the albino phenotype reappeared. The ALM1 gene is expressed mainly in young leaves. alm1 plants died as a consequence of excessive reactive oxygen accumulation after the third-leaf stage. A series of biochemical assays verified that ALM1 interacted with the OsTrxz protein, which is one of the components of plastid-encoded RNA polymerase (PEP) complexes. A western blot experiment indicated that ALM1 played an important role in stabilizing OsTrxz in rice. An overexpression test of ALM1 revealed that ALM1 can increase drought resistance by removing excess reactive oxygen in rice seedlings. This study suggests that ALM1 not only participates in rice chloroplast biogenesis, but also increases rice stress resistance by scavenging excess reactive oxygen.

Keywords

Drought stressRiceChloroplast biogenesisPEP complex

References

[1]

K. Kusumi, A. Yara, N. Mitsui, Y. Tozawa, K. Iba, Characterization of a rice nuclear-encoded plastid RNA polymerase geneOsRpoTp, Plant Cell Physiol 45 (2004) 1194-1201.
Crossref Google Scholar
[2]

E. Gantt, Oxygenic photosynthesis and the distribution of chloroplasts, Photosynth. Res. 107 (2011) 1-6.
Crossref Google Scholar
[3]

X. Liang, X. Liang, D. Qiao, M. Huang, X. Yi, L. Bai, H. Xu, L. Wei, J. Zeng, Y.i. Cao, Identification of a gene encoding the light-harvesting chlorophyll a / b proteins of photosystem Ⅰ in green alga Dunaliella salina, DNA Sequence 19 (2008) 137-145.
Crossref Google Scholar
[4]

X. Cui, Y. Wang, J. Wu, X. Han, X. Gu, T. Lu, Z. Zhang, The RNA editing factor DUA1 is crucial to chloroplast development at low temperature in rice, New Phytol. 221 (2019) 834-849.
Crossref Google Scholar
[5]

J. Kim, Y.J. Na, S.J. Park, S.H. Baek, D.H. Kim, Biogenesis of chloroplast outer envelope membrane proteins, Plant Cell Rep. 38 (2019) 783-792.
Crossref Google Scholar
[6]

V. Shanmugabalaji, H. Chahtane, S. Accossato, M. Rahire, G. Gouzerh, L. Lopez-Molina, F. Kessler, Chloroplast biogenesis controlled by DELLA-TOC159 interaction in early plant development, Curr. Biol. 28 (2018) 2616-2623.e5.
Crossref Google Scholar
[7]

C.Y. Yoo, E.K. Pasoreck, H. Wang, J. Cao, G.M. Blaha, D. Weigel, M. Chen, Phytochrome activates the plastid-encoded RNA polymerase for chloroplast biogenesis via nucleus-to-plastid signaling, Nat. Commun. 10 (2019) 2629.
Crossref Google Scholar
[8]

N. Gonzalez-Schain, I. Roig-Villanova, M.M. Kater, Early cold stress responses in post-meiotic anthers from tolerant and sensitive rice cultivars, Rice 12 (2019) 94.
Crossref Google Scholar
[9]

V. Ambastha, G. Chauhan, B.S. Tiwari, B.C. Tripathy, Execution of programmed cell death by singlet oxygen generated inside the chloroplasts of Arabidopsis thaliana, Protoplasma 257 (2020) 841-851.
Crossref Google Scholar
[10]

A. Schmidt, R. Mächtel, A. Ammon, T. Engelsdorf, J. Schmitz, V.G. Maurino, L.M. Voll, Reactive oxygen species dosage in Arabidopsis chloroplasts can improve resistance towards Colletotrichum higginsianum by the induction of WRKY33, New Phytol. 226 (2020) 189-204.
Crossref Google Scholar
[11]

T. Karuppanapandian, J.C. Moon, C. Kim, K. Manoharan, W. Kim, Reactive oxygen species in plants: their generation, signal transduction, and scavenging mechanisms, Aust. J. Crop Sci. 5 (2011) 709-725.
Google Scholar
[12]

R. Mittler, Oxidative stress, antioxidants and stress tolerance, Trends Plant Sci. 7 (2002) 405-410.
Crossref Google Scholar
[13]

C.H. Foyer, G. Noctor, Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses, Plant Cell 17 (2005) 1866-1875.
Crossref Google Scholar
[14]

R.G. Alscher, N. Erturk, L.S. Heath, Role of superoxide dismutases (SODs) in controlling oxidative stress in plants, J. Exp. Bot. 53 (2002) 1331-1341.
Crossref Google Scholar
[15]

Z. Zhang, Q. Zhang, J. Wu, X. Zheng, S. Zheng, X. Sun, Q. Qiu, T. Lu, Gene knockout study reveals that cytosolic ascorbate peroxidase 2 (OsAPX2) plays a critical role in growth and reproduction in rice under drought, salt and cold stresses, PLoS ONE (2013) e57472.
Crossref Google Scholar
[16]

X. Zheng, D.X. Tan, A.C. Allan, B. Zuo, Y. Zhao, R.J. Reiter, L. Wang, Z. Wang, Y. Guo, J. Zhou, D. Shan, Q. Li, Z. Han, J. Kong, Chloroplastic biosynthesis of melatonin and its involvement in protection of plants from salt stress, Sci. Rep. 7 (2017) 41236.
Crossref Google Scholar
[17]

W. Sun, B. Wang, X.L. Qu, B.Q. Zheng, W.D. Huang, Z.W. Sun, C.M. Wang, Y. Chen, Metabolism of reactive oxygen species in osteosarcoma and potential treatment applications, Cells 9 (2019) 87.
Crossref Google Scholar
[18]

M.A. Ferrer, M.A. Pedreno, R. Munoz, A.R. Barcelo, Oxidation of coniferyl alcohol by cell wall peroxidases at the expense of indole-3-acetic acid and O2: a model for the lignification of plant cell walls in the absence of H2O2, FEBS Lett 276 (1990) 127-130.
Crossref Google Scholar
[19]

W. Jiang, L. Yang, Y. He, H. Zhang, W. Li, H. Chen, D. Ma, J. Yin, Genome-wide identification and transcriptional expression analysis of superoxide dismutase (SOD) family in wheat (Triticum aestivum), PeerJ 7 (2019) e8062.
Crossref Google Scholar
[20]

Z.B. Liu, W.J Zhang, X.D. Gong, Q. Zhang, L.R. Zhou, A Cu/Zn superoxide dismutase from Jatropha curcas enhances salt tolerance of Arabidopsis thaliana, Genet. Mol. Res. 14 (2015) 2086-2098.
Crossref Google Scholar
[21]

A. Shafi, T. Gill, Y. Sreenivasulu, S. Kumar, P.S. Ahuja, A.K. Singh, Improved callus induction, shoot regeneration, and salt stress tolerance in Arabidopsis overexpressing superoxide dismutase from Potentilla atrosanguinea, Protoplasma 252 (2015) 41-51.
Crossref Google Scholar
[22]

S. Wan, J. Wu, Z. Zhang, X. Sun, Y. Lv, C.i. Gao, Y. Ning, J. Ma, Y. Guo, Q. Zhang, X. Zheng, C. Zhang, Z. Ma, T. Lu, Activation tagging, an efficient tool for functional analysis of the rice genome, Plant Mol. Biol. 69 (2009) 69-80.
Crossref Google Scholar
[23]

D.I. Arnon, Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris, Plant Physiol. 24 (1949) 1-15.
Crossref Google Scholar
[24]

Y. Hiei, S. Ohta, T. Komari, T. Kumashiro, Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA, Plant J. 6 (1994) 271-282.
Crossref Google Scholar
[25]

X. Ma, Q. Zhang, Q. Zhu, W. Liu, Y. Chen, R. Qiu, B. Wang, Z. Yang, H. Li, Y. Lin, Y. Xie, R. Shen, S. Chen, Z. Wang, Y. Chen, J. Guo, L. Chen, X. Zhao, Z. Dong, Y.G. Liu, A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants, Mol. Plant 8 (2015) 1274-1284.
Crossref Google Scholar
[26]

Y. Zhang, J. Su, S. Duan, Y. Ao, J. Dai, J. Liu, P. Wang, Y. Li, B. Liu, D. Feng, J. Wang, H. Wang, A highly efficient rice green tissue protoplast system for transient gene expression and studying light/chloroplast-related processes, Plant Methods 7 (2011) 30.
Crossref Google Scholar
[27]

R. Waadt, L.K. Schmidt, M. Lohse, K. Hashimoto, R. Bock, J. Kudla, Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta, Plant J. 56 (2008) 505–516.
Crossref Google Scholar
[28]

K.J. Livak, T.D. Schmittgen, Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method, Methods 25 (2001) 402-408.
Crossref Google Scholar
[29]

B.G. Hall, Building phylogenetic trees from molecular data with MEGA, Mol. Biol. Evol. 30 (2013) 1229-1235.
Crossref Google Scholar
[30]

G. Frahry, P. Schopfer, NADH stimulated, cyanide resistant superoxide production in maize coleoptiles analyzed with tetrazolium based assay, Planta 212 (2001) 175-183.
Crossref Google Scholar
[31]

H. Thordal-Christensen, Z. Zhang, Y. Wei, D.B. Collinge, Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction, Plant J 11 (1997) 1187-1194.
Crossref Google Scholar
[32]

Y. Lv, G. Shao, J. Qiu, G. Jiao, Z. Sheng, L. Xie, Y. Wu, S. Tang, X. Wei, P. Hu, White Leaf and Panicle 2, encoding a PEP-associated protein, is required for chloroplast biogenesis under heat stress in rice, J. Exp. Bot. 68 (2017) 5147-5160.
Crossref Google Scholar
[33]

J. Pfalz, K. Liere, A. Kandlbinder, K.J. Dietz, R. Oelmüller, pTAC2, -6, and -12 Are components of the transcriptionally active plastid chromosome that are required for plastid gene expression, Plant Cell 18 (2006) 176-197.
Crossref Google Scholar
[34]

AL. Chateigner-Boutin, M. Ramos-Vega, A. Guevara-García, C. Andrés, ML. Gutiérrez-Nava, A. Cantero, E. Delannoy, LF. Jiménez, C. Lurin, I. Small, P. León, CLB19, a pentatricopeptide repeat protein required for editing of rpoA and clpP chloroplast transcripts, Plant J 54 (2008) 590-602.
Crossref Google Scholar
[35]

A.L. Chateigner-Boutin, C.C. Francs-Small, E. Delannoy, S. Kahlau, S.K. Tanz, A.F. Longevialle, S. Fujii, I. Small, OTP70 is a pentatricopeptide repeat protein of the E subgroup involved in splicing of the plastid transcript rpoC1, Plant J. 65 (2011) 532-542.
Crossref Google Scholar
[36]

J. Wu, Z. Zhang, Q. Zhang, X. Han, X. Gu, T. Lu, The molecular cloning and clarification of a photorespiratory mutant, oscdm1, using enhancer trapping, Front. Genet. 6 (2015) 226.
Crossref Google Scholar
[37]

Y. Zhao, H. Yu, J.M. Zhou, S.M. Smith, J. Li, Malate circulation: linking chloroplast metabolism to mitochondrial ROS, Trends Plant Sci. 25 (2020) 446-454.
Crossref Google Scholar
[38]

A. Lokdarshi, J.u. Guan, R.A. Urquidi Camacho, S.K. Cho, P.W. Morgan, M. Leonard, M. Shimono, B. Day, A.G. von Arnim, Light activates the translational regulatory kinase GCN2 via reactive oxygen species emanating from the chloroplast, Plant Cell 32 (2020) 1161-1178.
Crossref Google Scholar
[39]

V. Dogra, M. Li, S. Singh, M. Li, C. Kim, Oxidative post-translational modification of EXECUTER1 is required for singlet oxygen sensing in plastids, Nat. Commun. 10 (2019) 2834.
Crossref Google Scholar
[40]

F. Myouga, C. Hosoda, T. Umezawa, H. Iizumi, T. Kuromori, R. Motohashi, Y. Shono, N. Nagata, M. Ikeuchi, K. Shinozaki, A heterocomplex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in arabidopsis, Plant Cell 20 (2008) 3148-3162.
Crossref Google Scholar
[41]

Z. Zhang, X. Cui, Y. Wang, J. Wu, X. Gu, T. Lu, The RNA editing factor WSP1 is essential for chloroplast development in rice, Mol. Plant 10 (2017) 86-98.
Crossref Google Scholar
[42]

L. He, S. Zhang, Z. Qiu, J. Zhao, W. Nie, H. Lin, Z. Zhu, D. Zeng, Q. Qian, L. Zhu, Fructokinase-like protein 1 interacts with TRXz to regulate chloroplast development in rice, J. Integr. Plant Biol. 60 (2018) 94-111.
Crossref Google Scholar
[43]

J. Sun, T. Zheng, J. Yu, T. Wu, X. Wang, G. Chen, Y. Tian, H. Zhang, Y. Wang, W. Terzaghi, C. Wang, J. Wan, TSV, a putative plastidic oxidoreductase, protects rice chloroplasts from cold stress during development by interacting with plastidic thioredoxin Z, New Phytol. 215 (2017) 240-255.
Crossref Google Scholar
The Crop Journal
Volume 9 Issue 5,
October 2021
Pages 1018-1029
DOI: 10.1016/j.cj.2020.09.013
Cite this article:
Wang Y, Deng C, Ai P, et al. ALM1, encoding a Fe-superoxide dismutase, is critical for rice chloroplast biogenesis and drought stress response. The Crop Journal, 2021, 9(5): 1018-1029. https://doi.org/10.1016/j.cj.2020.09.013

302

Views

3

Downloads

18

Crossref

N/A

Web of Science

16

Scopus

2

CSCD

Altmetrics
Received: 15 May 2020
Revised: 16 September 2020
Accepted: 27 November 2020
Published: 18 December 2020
© 2020 Crop Science Society of China and Institute of Crop Science, CAAS.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Return