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 (5.2 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

A valine residue deletion in ZmSig2A, a sigma factor, accounts for a revertible leaf-color mutation in maize

Chuan Lia,1, Jingwen Wanga,1, Zhaoyong Hua, Yuanyan Xiaa, Qiang Huanga, Tao Yua, Hongyang Yia, Yanli Lua,b, Jing Wanga, Moju Caoa,b( )
Maize Research Institute, Sichuan Agricultural University, Chengdu 611130, Sichuan, China
State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Chengdu 611130, Sichuan, China

1 These authors contributed equally to this work.

Show Author Information

Abstract

A nuclear-encoded sigma (σ) factor is essential for the transcriptional regulation of plant chloroplast-encoded genes. Five putative maize σ factors have been identified by database searches, but their functions are unknown. We report a maize leaf color mutant etiolated/albino leaf 1 (eal1) that was derived from space mutation breeding. The eal1 mutant displays etiolated or albino leaves that then gradually turn to normal green at the seedling stage. The changes in eal1 leaf color are associated with changes in photosynthetic pigment content and chloroplast development. Map-based cloning revealed that a single amino-acid deletion changing Val480-Val481-Val482 to Val480-Val481, in the C-terminal domain σ4 of the putative σ factor ZmSig2A, is responsible for the eal1 mutation. In comparison with the expression level of the wild-type (WT) allele ZmSig2A+ in WT plants, much higher expression of the mutant allele ZmSig2AΔV in eal1 plants was detected before the eal1 plants turned to normal green. ZmSig2A shows the highest similarity to rice OsSig2A and Arabidopsis SIG2. Ectopic expression of ZmSig2A+ or ZmSig2AΔV driven by the cauliflower mosaic virus 35S promoter rescued the pale green leaf of the sig2 mutant, but ectopic expression of ZmSig2AΔV driven by the SIG2 promoter did not. We propose that the Val deletion generated a new weak allele of ZmSig2A that cannot completely abolish the ZmSig2A function. Some genes involved in chloroplast development and photosynthesis-associated nuclear genes showed significant expression differences between eal1 and WT plants. We conclude that ZmSig2A encoding a σ factor is essential for maize chloroplast development. The eal1 mutant with a weak allele of ZmSig2A represents a valuable genetic resource for investigating the regulation of ZmSig2A-mediated chloroplast development in maize. The eal1 mutation may be useful as a marker for early identification and elimination of false hybrids or transgene transmission in the application of genetic male sterility to commercial hybrid seed production.

Keywords

MaizeChloroplast developmentLeaf color mutantMap-based cloningSigma factor

References

[1]

H.E. Neuhaus, M.J. Emes, Nonphotosynthetic metabolism in plastids, Annu. Rev. Plant Physiol. Plant Mol. Biol. 51 (2000) 111-140.
Crossref Google Scholar
[2]

M.T. Waters, J.A. Langdale, The making of a chloroplast, EMBO J. 28 (2009) 2861-2873.
Crossref Google Scholar
[3]

A. Barkan, Studying the structure and processing of chloroplast transcripts, Methods Mol. Biol. 774 (2011) 183-197.
Crossref Google Scholar
[4]

Q.B. Yu, C. Huang, Z.N. Yang, Nuclear-encoded factors associated with the chloroplast transcription machinery of higher plants, Front. Plant Sci. 5 (2014) 316.
Crossref Google Scholar
[5]

T. Börner, A.Y. Aleynikova, Y.O. Zubo, V.V. Kusnetsov, Chloroplast RNA polymerases: role in chloroplast biogenesis, Biochim. Biophys. Acta. 1847 (2015) 761-769.
Crossref Google Scholar
[6]

L.A. Macadlo, I.M. Ibrahim, S. Puthiyaveetil, Sigma factor 1 in chloroplast gene transcription and photosynthetic light acclimation, J. Exp. Bot. 71 (2020) 1029-1038.
Crossref Google Scholar
[7]

F. Hu, Y. Zhu, W. Wu, Y.e. Xie, J. Huang, Leaf variegation of thylakoid formation1 is suppressed by mutations of specific σ-factors in Arabidopsis, Plant Physiol. 168 (2015) 1066-1075.
Crossref Google Scholar
[8]

W. Zghidi, L. Merendino, A. Cottet, R. Mache, S. Lerbs-Mache, Nucleus-encoded plastid sigma factor SIG3 transcribes specifically the psbN gene in plastids, Nucleic Acids Res. 35 (2007) 455-464.
Crossref Google Scholar
[9]

M. Malik Ghulam, O. Zghidi-Abouzid, E. Lambert, S. Lerbs-Mache, L. Merendino, Transcriptional organization of the large and the small ATP synthase operons, atpI/H/F/A and atpB/E, in Arabidopsis thaliana chloroplasts, Plant Mol. Biol. 79 (2012) 259-272.
Crossref Google Scholar
[10]

J.J. Favory, M. Kobayshi, K. Tanaka, G. Peltier, M. Kreis, J.G. Valay, S. Lerbs-Mache, Specific function of a plastid sigma factor for ndhF gene transcription, Nucleic Acids Res. 33 (2005) 5991-5999.
Crossref Google Scholar
[11]

Y. Tsunoyama, Y. Ishizaki, K. Morikawa, M. Kobori, Y. Nakahira, G. Takeba, Y. Toyoshima, T. Shiina, Blue light-induced transcription of plastid-encoded psbD gene is mediated by a nuclear-encoded transcription initiation factor, AtSig5, Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 3304-3309.
Crossref Google Scholar
[12]

Z.B. Noordally, K. Ishii, K.A. Atkins, S.J. Wetherill, J. Kusakina, E.J. Walton, M. Kato, M. Azuma, K. Tanaka, M. Hanaoka, A.N. Dodd, Circadian control of chloroplast transcription by a nuclear-encoded timing signal, Science 339 (2013) 1316-1319.
Crossref Google Scholar
[13]

Y. Ishizaki, Y. Tsunoyama, K. Hatano, K. Ando, K. Kato, A. Shinmyo, M. Kobori, G. Takeba, Y. Nakahira, T. Shiina, A nuclear-encoded sigma factor, Arabidopsis SIG6, recognizes sigma-70 type chloroplast promoters and regulates early chloroplast development in cotyledons, Plant J. 42 (2005) 133-144.
Crossref Google Scholar
[14]

Y. Yu, Z. Zhou, H. Pu, B. Wang, Y. Zhang, B.O. Yang, T. Zhao, D. Xu, OsSIG2A is required for chloroplast development in rice (Oryza sativa L.) at low temperature by regulating plastid genes expression, Funct. Plant Biol. 46 (2019) 766-776.
Crossref Google Scholar
[15]

K. Kasai, M. Kawagishi-Kobayashi, M. Teraishi, Y. Ito, K. Ochi, K. Wakasa, Y. Tozawa, Differential expression of three plastidial sigma factors, OsSIG1, OsSIG2A, and OsSIG2B, during leaf development in rice, Biosci. Biotechnol. Biochem. 68 (2004) 973-977.
Crossref Google Scholar
[16]

Y. Tozawa, M. Teraishi, T. Sasaki, K. Sonoike, Y. Nishiyama, M. Itaya, A. Miyao, H. Hirochika, The plastid sigma factor SIG1 maintains photosystem I activity via regulated expression of the psaA operon in rice chloroplasts, Plant J. 52 (2007) 124-132.
Crossref Google Scholar
[17]

Y. Kubota, A. Miyao, H. Hirochika, Y. Tozawa, H. Yasuda, Y. Tsunoyama, Y. Niwa, S. Imamura, M. Shirai, M. Asayama, Two novel nuclear genes, OsSIG5 and OsSIG6, encoding potential plastid sigma factors of RNA polymerase in rice: tissue-specific and light-responsive gene expression, Plant Cell Physiol. 48 (2007) 186-192.
Crossref Google Scholar
[18]

S.D. Lahiri, J. Yao, C. McCumbers, L.A. Allison, Tissue-specific and light-dependent expression within a family of nuclear-encoded sigma-like factors from Zea mays, Mol. Cell Biol. Res. Commun. 1 (1999) 14-20.
Crossref Google Scholar
[19]

S. Tan, R.F. Troxler, Characterization of two chloroplast RNA polymerase sigma factors from Zea mays: photoregulation and differential expression, Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 5316-5321.
Crossref Google Scholar
[20]

T.A. Beardslee, S. Roy-Chowdhury, P. Jaiswal, L. Buhot, S. Lerbs-Mache, D.B. Stern, L.A. Allison, A nucleus-encoded maize protein with sigma factor activity accumulates in mitochondria and chloroplasts, Plant J. 31 (2002) 199-209.
Crossref Google Scholar
[21]

S.D. Lahiri, L.A. Allison, Complementary expression of two plastid-localized sigma-like factors in maize, Plant Physiol. 123 (2000) 883-894.
Crossref Google Scholar
[22]

D. Shi, X.u. Zheng, L. Li, W. Lin, W. Xie, J. Yang, S. Chen, W. Jin, J.H. Liu, Chlorophyll deficiency in the maize elongated mesocotyl2 mutant is caused by a defective heme oxygenase and delaying grana stacking, PLoS ONE 8 (2013) e80107.
Crossref Google Scholar
[23]

X. Zhu, S. Liang, J. Yin, C. Yuan, J. Wang, W. Li, M. He, J. Wang, W. Chen, B. Ma, Y. Wang, P. Qin, S. Li, X. Chen, The DnaJ OsDjA7/8 is essential for chloroplast development in rice (Oryza sativa), Gene 574 (2015) 11-19.
Crossref Google Scholar
[24]

P. Horton, K.J. Park, T. Obayashi, N. Fujita, H. Harada, C.J. Adams-Collier, K. Nakai, WoLF PSORT: protein localization predictor, Nucleic Acids Res. 35 (2007) W585-W587.
Crossref Google Scholar
[25]

K.C. Chou, H.B. Shen, Large-scale plant protein subcellular location prediction, J. Cell Biochem. 100 (2007) 665-678.
Crossref Google Scholar
[26]

L.A. Kelley, S. Mezulis, C.M. Yates, M.N. Wass, M.J.E. Sternberg, The Phyre2 web portal for protein modeling, prediction and analysis, Nat. Protoc. 10 (2015) 845-858.
Crossref Google Scholar
[27]

S. Kumar, G. Stecher, M. Li, C. Knyaz, K. Tamura, MEGA X: molecular evolutionary genetics analysis across computing platforms, Mol. Biol. Evol. 35 (2018) 1547-1549.
Crossref Google Scholar
[28]

R.C. Edgar, MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic Acids Res. 32 (2004) 1792-1797.
Crossref Google Scholar
[29]

L. Liu, Y. Zhang, S. Tang, Q. Zhao, Z. ZhanG, H. Zhang, L. Dong, H. Guo, Q. Xie, An efficient system to detect protein ubiquitination by agroinfiltration in Nicotiana benthamiana, Plant J. 61 (2010) 893-903.
Crossref Google Scholar
[30]

S.J. Clough, A.F. Bent, Floral dip: a simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana, Plant J. 16 (1998) 735-743.
Crossref Google Scholar
[31]

H. Du, X. Shen, Y. Huang, M. Huang, Z. Zhang, Overexpression of Vitreoscilla hemoglobin increases waterlogging tolerance in Arabidopsis and maize, BMC Plant Biol. 16 (2016) 35.
Crossref Google Scholar
[32]

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
[33]

S.R. Kim, G. An, Rice chloroplast-localized heat shock protein 70, OsHsp70CP1, is essential for chloroplast development under high-temperature conditions, J. Plant Physiol. 170 (2013) 854-863.
Crossref Google Scholar
[34]

X. Liu, J. Lan, Y. Huang, P. Cao, C. Zhou, Y. Ren, N. He, S. Liu, Y. Tian, T. Nguyen, L. Jiang, J. Wan, WSL5, a pentatricopeptide repeat protein, is essential for chloroplast biogenesis in rice under cold stress, J. Exp. Bot. 69 (2018) 3949-3961.
Crossref Google Scholar
[35]

X. Zhu, M. Ze, J. Yin, M. Chern, M. Wang, X. Zhang, R. Deng, Y. Li, H. Liao, L. Wang, B. Tu, L. Song, M. He, S. Li, W. Wang, X. Chen, J. Wang, W. Li, A phosphofructokinase B-type carbohydrate kinase family protein, PFKB1, is essential for chloroplast development at early seedling stage in rice, Plant Sci. 290 (2020) 110295.
Crossref Google Scholar
[36]

E.A. Lysenko, Plant sigma factors and their role in plastid transcription, Plant Cell Rep. 26 (2007) 845-859.
Crossref Google Scholar
[37]

E.A. Campbell, O. Muzzin, M. Chlenov, J.L. Sun, C.A. Olson, O. Weinman, M.L. Trester-Zedlitz, S.A. Darst, Structure of the bacterial RNA polymerase promoter specificity sigma subunit, Mol. Cell 9 (2002) 527-539.
Crossref Google Scholar
[38]

W. Chi, B. He, J. Mao, J. Jiang, L. Zhang, Plastid sigma factors: Their individual functions and regulation in transcription, Biochim. Biophys. Acta 2015 (1847) 770-778.
Crossref Google Scholar
[39]

J.D. Woodson, J.M. Perez-Ruiz, R.J. Schmitz, J.R. Ecker, J. Chory, Sigma factor-mediated plastid retrograde signals control nuclear gene expression, Plant J. 73 (2013) 1-13.
Crossref Google Scholar
[40]

S.L. Dove, S.A. Darst, A. Hochschild, Region 4 of sigma as a target for transcription regulation, Mol. Microbiol. 48 (2003) 863-874.
Crossref Google Scholar
[41]

U.K. Sharma, D. Chatterji, Both regions 4.1 and 4.2 of E. coli sigma (70) are together required for binding to bacteriophage T4 AsiA in vivo, Gene 376 (2006) 133-143.
Crossref Google Scholar
[42]

J.D. Woodson, J. Chory, Coordination of gene expression between organellar and nuclear genomes, Nat. Rev. Genet. 9 (2008) 383-395.
Crossref Google Scholar
[43]

J.H. Lukens, D.E. Mathews, R.D. Durbin, Effect of tagetitoxin on the levels of ribulose 1,5-bisphosphate carboxylase, ribosomes, and RNA in plastids of wheat leaves, Plant Physiol. 84 (1987) 808-813.
Crossref Google Scholar
[44]

J.C. Rapp, J.E. Mullet, Chloroplast transcription is required to express the nuclear genes rbcS and cab. Plastid DNA copy number is regulated independently, Plant Mol. Biol. 17 (1991) 813-823.
Crossref Google Scholar
[45]

T. Pfannschmidt, G. Link, The A and B forms of plastid DNA-dependent RNA polymerase from mustard (Sinapis alba L.) transcribe the same genes in a different developmental context, Mol. Gen. Genet. 257 (1997) 35-44.
Crossref Google Scholar
[46]

X.G. Zhu, S.P. Long, D.R. Ort, Improving photosynthetic efficiency for greater yield, Annu. Rev. Plant Biol. 61 (2010) 235-261.
Crossref Google Scholar
[47]

Y. Wu, T.W. Fox, M.R. Trimnell, L. Wang, R.J. Xu, A.M. Cigan, G.A. Huffman, C.W. Garnaat, H. Hershey, M.C. Albertsen, Development of a novel recessive genetic male sterility system for hybrid seed production in maize and other cross-pollinating crops, Plant Biotechnol. J. 14 (2016) 1046-1054.
Crossref Google Scholar
[48]
Zhang D. Wu S. An X. Xie K.E. Dong Z. Zhou Y. Xu L. Fang W. Liu S. Liu S. Zhu T. Li J. Rao L. Zhao J. Wan X. Construction of a multicontrol sterility system for a maize male-sterile line and hybrid seed production based on the ZmMs7 gene encoding a PHD-finger transcription factorPlant Biotechnol.  J.20181645947110.1111/pbi.12786

D. Zhang, S. Wu, X. An, K.E. Xie, Z. Dong, Y. Zhou, L. Xu, W. Fang, S. Liu, S. Liu, T. Zhu, J. Li, L. Rao, J. Zhao, X. Wan, Construction of a multicontrol sterility system for a maize male-sterile line and hybrid seed production based on the ZmMs7 gene encoding a PHD-finger transcription factor, Plant Biotechnol.  J. 16 (2018) 459-471.
Crossref Google Scholar
The Crop Journal
Volume 9 Issue 6,
December 2021
Pages 1330-1343
DOI: 10.1016/j.cj.2021.01.005
Cite this article:
Li C, Wang J, Hu Z, et al. A valine residue deletion in ZmSig2A, a sigma factor, accounts for a revertible leaf-color mutation in maize. The Crop Journal, 2021, 9(6): 1330-1343. https://doi.org/10.1016/j.cj.2021.01.005

245

Views

4

Downloads

7

Crossref

7

Web of Science

7

Scopus

0

CSCD

Altmetrics
Received: 26 August 2020
Revised: 11 December 2020
Accepted: 29 January 2021
Published: 13 March 2021
© 2021 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