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Proteome alterations of reverse photoperiod-sensitive genic male sterile rice (Oryza sativa L.) at fertility transformation stage

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Abstract

The two-line system has been widely used in hybrid rice seed production, and the reverse photoperiod-sensitive genic male sterile line is a new germplasm with an opposite phenotype compared with normal photoperiod-sensitive genic male sterile rice. To better understand the molecular mechanisms of fertility regulation in reverse photoperiod-sensitive genic male sterile rice, a comparative proteomic approach was used to analyze the protein profiles of three different tissues (young panicles, flag leaves and leaf sheaths) of D52S during the sensitive period of pollen fertility transformation under sterile and fertile conditions. By quantitative analysis, 66 protein spots were identified to be significantly changed in the three tissues. Bioinformatics analyses revealed that in sterile rice, a number of proteins involved in lignin-flavonoid biosynthesis pathway were down-accumulated in panicles. The majority of proteins associated with energy metabolism were down-accumulated in leaf sheaths while the proteins up-accumulated in leaves and leaf sheaths were exclusively photosynthesis and defense related. Based on the proteomics data, a short-day induced male sterility protein network was proposed. In addition, the genes of selected protein spots were further analyzed by qPCR. These findings provide data for better understanding the regulation of pollen fertility in reverse photoperiod-sensitive genic male sterile rice, which could assist in the development of practical reverse photoperiod-sensitive genic male sterile rice for large-scale crop breeding programs.

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Abbreviations

β-met:

Beta-mercaptoethanol

LD:

Long-day length

SD:

Short-day length

RPGMS:

Reverse photoperiod-sensitive genic male sterile

EGMS:

Environmentally sensitive genetic male sterile

PGMS:

Photoperiod-sensitive genic male sterile

TGMS:

Thermo-sensitive genic male sterile

NPK:

N:P2O5:K2O

References

  • Agrawal GK, Rakwal R (2011) Rice proteomics: a move toward expanded proteome coverage to comparative and functional proteomics uncovers the mysteries of rice and plant biology. Proteomics 11:1630–1649

    Article  CAS  PubMed  Google Scholar 

  • Austin MB, Noel JP (2003) The chalcone synthase superfamily of type III polyketide synthases. Nat Prod Rep 20:79–110

    Article  CAS  PubMed  Google Scholar 

  • Bevan M, Bancroft I, Bent E, Love K, Goodman H, Dean C, Bergkamp R, Dirkse W, Van Staveren M, Stiekema W (1998) Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature 391:485–488

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Chen LY, Xiao YH, Lei DY (2010) Mechanism of sterility and breeding strategies for photoperiod/thermo-sensitive genic male sterile rice. Rice Sci 17:161–167

    Article  CAS  Google Scholar 

  • Chen RZ, Zhao X, Shao Z, Wei Z, Wang YY, Zhu LL, Zhao J, Sun MX, He RF, He GC (2007) Rice UDP-glucose pyrophosphorylase1 is essential for pollen callose deposition and its cosuppression results in a new type of thermosensitive genic male sterility. Plant Cell 19:847–861

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen X, Hu J, Zhang H, Ding Y (2014) DNA methylation changes in photoperiod-thermo-sensitive male sterile rice PA64S under two different conditions. Gene 537:143–148

    Article  CAS  PubMed  Google Scholar 

  • Cheng LB, Gao XA, Li SY, Shi MJ, Javeed H, Jing XM, Yang GX, He GY (2010) Proteomic analysis of soybean [Glycine max (L.) Meer.] seeds during imbibition at chilling temperature. Mol Breed 26:1–17

    Article  CAS  Google Scholar 

  • Cheng SH, Zhuang JY, Fan YY, Du JH, Cao LY (2007) Progress in research and development on hybrid rice: a super-domesticate in China. Ann Bot 100:959–966

    Article  PubMed Central  PubMed  Google Scholar 

  • Collman JP, Boulatov R, Sunderland CJ, Fu L (2004) Functional analogues of cytochrome c oxidase, myoglobin, and hemoglobin. Chem Rev 104:561–588

    Article  CAS  PubMed  Google Scholar 

  • Datta R, Chourey PS, Pring DR, Tang HV (2001) Gene-expression analysis of sucrose-starch metabolism during pollen maturation in cytoplasmic male-sterile and fertile lines of sorghum. Sex Plant Reprod 14:127–134

    Article  CAS  Google Scholar 

  • Denecke J, Goldman M, Demolder J, Seurinck J, Botterman J (1991) The tobacco luminal binding protein is encoded by a multigene family. Plant Cell 3:1025–1035

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ding JH, Lu Q, Ouyang YD, Mao HL, Zhang PB, Yao JL, Xu CG, Li XH, Xiao JH, Zhang QF (2012) A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc Natl Acad Sci 109:2654–2659

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dobritsa AA, Lei ZT, Nishikawa S-i, Urbanczyk-Wochniak E, Huhman DV, Preuss D, Sumner LW (2010) LAP5 and LAP6 encode anther-specific proteins with similarity to chalcone synthase essential for pollen exine development in Arabidopsis. Plant Physiol 153:937–955

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fujii S, Komatsu S, Toriyama K (2007) Retrograde regulation of nuclear gene expression in CW-CMS of rice. Plant Mol Biol 63:405–417

    Article  CAS  PubMed  Google Scholar 

  • Ge P, Ma C, Wang S, Gao L, Li X, Guo G, Ma W, Yan Y (2012) Comparative proteomic analysis of grain development in two spring wheat varieties under drought stress. Anal Bioanal Chem 402:1297–1313

    Article  CAS  PubMed  Google Scholar 

  • Gibon Y, Bläsing OE, Palacios-Rojas N, Pankovic D, Hendriks JH, Fisahn J, Höhne M, Günther M, Stitt M (2004) Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period. Plant J 39:847–862

    Article  CAS  PubMed  Google Scholar 

  • Goh C-H, Ko S-M, Koh S, Kim Y-J, Bae H-J (2012) Photosynthesis and environments: photoinhibition and repair mechanisms in plants. J Plant Biol 55:93–101

    Article  CAS  Google Scholar 

  • Golding B, Liu X, Li XH, Zhang X, Wang SW (2010) Genetic analysis and mapping of a thermosensitive genic male sterility gene, tms6 (t), in rice (Oryza sativa L.). Genome 53:119–124

    Article  Google Scholar 

  • Goyer A (2010) Thiamine in plants: aspects of its metabolism and functions. Phytochemistry 71:1615–1624

    Article  CAS  PubMed  Google Scholar 

  • Grosshans BL, Ortiz D, Novick P (2006) Rabs and their effectors: achieving specificity in membrane traffic. Proc Natl Acad Sci 103:11821–11827

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gui JS, Shen JH, Li LG (2011) Functional characterization of evolutionarily divergent 4-coumarate: coenzyme A ligases in rice. Plant Physiol 157:574–586

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Guo A, Zheng CX (2013) Female gametophyte development. J Plant Biol 56:345–356

    Article  Google Scholar 

  • Gutierrez-Carbonell E, Lattanzio G, Sagardoy R, Rodríguez-Celma J, Ríos Ruiz JJ, Matros A, Abadía A, Abadía J, López-Millán AF (2013) Changes induced by zinc toxicity in the 2-DE protein profile of sugar beet roots. J Proteomics 94:149–161

    Article  CAS  PubMed  Google Scholar 

  • Haigler CH, Ivanova-Datcheva M, Hogan PS, Salnikov VV, Hwang S, Martin K, Delmer DP (2001) Carbon partitioning to cellulose synthesis. Plant Mol Biol 47:29–51

    Article  CAS  PubMed  Google Scholar 

  • Hirose T, Scofield GN, Terao T (2008) An expression analysis profile for the entire sucrose synthase gene family in rice. Plant Sci 174:534–543

    Article  CAS  Google Scholar 

  • Hu MQ, Li LQ, Chao JB, Zhao YQ, Zhang ZY, Liang AH (2013) The acidic ribosomal protein P2 from Euplotes octocarinatus is phosphorylated at its N-terminal domain. Biochem Cell Biol 91:1–10

    Article  Google Scholar 

  • Imin N, Kerim T, Weinman JJ, Rolfe BG (2006) Low temperature treatment at the young microspore stage induces protein changes in rice anthers. Mol Cell Proteomics 5:274–292

    Article  CAS  PubMed  Google Scholar 

  • Islam N, Lonsdale M, Upadhyaya NM, Higgins TJ, Hirano H, Akhurst R (2004) Protein extraction from mature rice leaves for two-dimensional gel electrophoresis and its application in proteome analysis. Proteomics 4:1903–1908

    Article  CAS  PubMed  Google Scholar 

  • Joseph CA, Chen Z, Ma D, Zeng HL (2011) Analysis of short photo-periodic sensitive genic male sterility and molecular mapping of rpms3 (t) gene in rice (Oryza sativa L.) using SSR markers. Genes Genom 33:513–519

    Article  CAS  Google Scholar 

  • Kleczkowski LA (1994) Glucose activation and metabolism through UDP-glucose pyrophosphorylase in plants. Phytochemistry 37:1507–1515

    Article  CAS  Google Scholar 

  • Kobayashi T, Kobayashi E, Sato S, Hotta Y, Miyajima N, Tanaka A, Tabata S (1994) Characterization of cDNAs induced in meiotic prophase in lily microsporocytes. DNA Res 1:15–26

    Article  CAS  PubMed  Google Scholar 

  • Krampitz LO (1969) Catalytic functions of thiamin diphosphate. Annu Rev Biochem 38:213–240

    Article  CAS  PubMed  Google Scholar 

  • Lang NT, Subudhi PK, Virmani SS, Brar DS, Khush GS, Li ZK, Huang N (1999) Development of PCR-based markers for thermosensitive genetic male sterility gene tms3 (t) in rice (Oryza Sativa L.). Hereditas 131:121–127

    Article  CAS  PubMed  Google Scholar 

  • LeClere S, Rampey RA, Bartel B (2004) IAR4, a gene required for auxin conjugate sensitivity in Arabidopsis, encodes a pyruvate dehydrogenase E1α homolog. Plant Physiol 135:989–999

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li SL (2004) A study on fertility alteration in yichun in rice D38s with short photoperiod low temperature induced male sterile. J Yichun Univ (Nat Sci) 4:78–81

    CAS  Google Scholar 

  • Li H, Chen Z, Hu M, Wang Z, Hua H, Yin C, Zeng H (2011) Different effects of night versus day high temperature on rice quality and accumulation profiling of rice grain proteins during grain filling. Plant Cell Rep 30:1641–1659

    Article  CAS  PubMed  Google Scholar 

  • Li JJ, Pandeya D, Jo YD, Liu WY, Kang BC (2013) Reduced activity of ATP synthase in mitochondria causes cytoplasmic male sterility in chili pepper. Planta 237:1097–1109

    Article  CAS  PubMed  Google Scholar 

  • Li M, Sha A, Zhou X, Yang P (2012) Comparative proteomic analyses reveal the changes of metabolic features in soybean (Glycine max) pistils upon pollination. Sex Plant Reprod 25:281–291

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lu Q, Li XH, Guo D, Xu CG, Zhang Q (2005) Localization of pms3, a gene for photoperiod-sensitive genic male sterility, to a 28.4-kb DNA fragment. Mol Genet Genomics 273:507–511

    Article  CAS  PubMed  Google Scholar 

  • Ma YJ, Hendershot LM (2004) ER chaperone functions during normal and stress conditions. J Chem Neuroanat 28:51–65

    Article  CAS  PubMed  Google Scholar 

  • Moffatt BA, Wang L, Allen MS, Stevens YY, Qin W, Snider J, von Schwartzenberg K (2000) Adenosine kinase of Arabidopsis. Kinetic properties and gene expression. Plant Physiol 124:1775–1785

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Napoli CA, Fahy D, Wang H, Taylor LP (1999) white anther: A petunia mutant that abolishes pollen flavonol accumulation, induces male sterility, and is complemented by a chalcone synthase transgene. Plant Physiol 120:615–622

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Peng HF, Zhang ZF, Wu B, Chen XH, Zhang GQ, Zhang ZM, Wan BH, Lu YP (2008) Molecular mapping of two reverse photoperiod-sensitive genic male sterility genes (rpms1 and rpms2) in rice (Oryza sativa L.). Theor Appl Genet 118:77–83

    Article  CAS  PubMed  Google Scholar 

  • Pradet-Balade B, Boulmé F, Beug H, Müllner EW, Garcia-Sanz JA (2001) Translation control: bridging the gap between genomics and proteomics? Trends Biochem Sci 26:225–229

    Article  CAS  PubMed  Google Scholar 

  • Rawlings ND, Barrett AJ (1994) Families of serine peptidases. Method Enzymol 244:19–61

    Article  CAS  Google Scholar 

  • Reflinur Chin JH, Jang SM, Kim B, Lee J, Koh HJ (2012) QTLs for hybrid fertility and their association with female and male sterility in rice. Genes Genom 34:355–365

    Article  Google Scholar 

  • Samonte SO, Wilson LT, McClung AM, Tarpley L (2001) Seasonal dynamics of nonstructural carbohydrate partitioning in 15 diverse rice genotypes. Crop Sci 41:902–909

    Article  Google Scholar 

  • Schijlen EG, de Vos CR, Martens S, Jonker HH, Rosin FM, Molthoff JW, Tikunov YM, Angenent GC, van Tunen AJ, Bovy AG (2007) RNA interference silencing of chalcone synthase, the first step in the flavonoid biosynthesis pathway, leads to parthenocarpic tomato fruits. Plant Physiol 144:1520–1530

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schluter H, Apweiler R, Holzhutter HG, Jungblut PR (2009) Finding one’s way in proteomics: a protein species nomenclature. Chem Cent J 3:11

    Article  PubMed Central  PubMed  Google Scholar 

  • Sheoran IS, Saini HS (1996) Drought-induced male sterility in rice: changes in carbohydrate levels and enzyme activities associated with the inhibition of starch accumulation in pollen. Sex Plant Reprod 9:161–169

    Article  Google Scholar 

  • Shi YL, Zhao S, Yao JL (2009) Premature tapetum degeneration: a major cause of abortive pollen development in photoperiod sensitive genic male sterility in rice. J Integr Plant Biol 51:774–781

    Article  PubMed  Google Scholar 

  • Sun QP, Hu CF, Hu J, Li SQ, Zhu YG (2009) Quantitative proteomic analysis of CMS-related changes in Honglian CMS rice anther. Protein J 28:341–348

    Article  CAS  PubMed  Google Scholar 

  • Tan TW, Lu JK, Nie K, Deng L, Wang F (2010) Biodiesel production with immobilized lipase: a review. Biotechnol Adv 28:628–634

    Article  CAS  PubMed  Google Scholar 

  • Tschaplinski TJ, Standaert RF, Engle NL, Martin MZ, Sangha AK, Parks JM, Smith JC, Samuel R, Jiang N, Pu Y (2012) Down-regulation of the caffeic acid o-methyltransferase gene in switchgrass reveals a novel monolignol analog. Biotechnol Biofuels 5:1–15

    Article  Google Scholar 

  • Valledor L, Jorrín J (2011) Back to the basics: maximizing the information obtained by quantitative two dimensional gel electrophoresis analyses by an appropriate experimental design and statistical analyses. J Proteomics 74:1–18

    Article  CAS  PubMed  Google Scholar 

  • Van Der Meer IM, Stam ME, van Tunen AJ, Mol JN, Stuitje AR (1992) Antisense inhibition of flavonoid biosynthesis in petunia anthers results in male sterility. Plant Cell 4:253–262

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang B, Xu WW, Wang JZ, Wu W, Zheng HG, Yang ZY, Ray JD, Nguyen HT (1995) Tagging and mapping the thermo-sensitive genic male-sterile gene in rice (Oryza sativa L.) with molecular markers. Theor Appl Genet 91:1111–1114

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Liu ZW, Guo ZB, Song GY, Cheng Q, Jiang DM, Zhu YG, Yang DC (2011) Comparative transcriptomes profiling of photoperiod-sensitive male sterile rice Nongken 58S during the male sterility transition between short-day and long-day. BMC Genome 12:462

    Article  CAS  Google Scholar 

  • Wang D, Oses-Prieto JA, Li KH, Fernandes JF, Burlingame AL, Walbot V (2010) The male sterile 8 mutation of maize disrupts the temporal progression of the transcriptome and results in the mis-regulation of metabolic functions. Plant J 63:939–951

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang K, Peng XJ, Ji YX, Yang PF, Zhu YG, Li SQ (2013) Gene, protein, and network of male sterility in rice. Front Plant Sci 4:92

    PubMed Central  PubMed  Google Scholar 

  • Wang YG, Xing QH, Deng QY, Liang FS, Yuan LP, Weng ML, Wang B (2003) Fine mapping of the rice thermo-sensitive genic male-sterile gene tms5. Theor Appl Genet 107:917–921

    Article  CAS  PubMed  Google Scholar 

  • Wei MM, Song MZ, Fan SL, Yu SX (2013) Transcriptomic analysis of differentially expressed genes during anther development in genetic male sterile and wild type cotton by digital gene-expression profiling. BMC Genomic 14:97

    Article  CAS  Google Scholar 

  • Weigelt K, Küster H, Rutten T, Fait A, Fernie AR, Miersch O, Wasternack C, Emery RN, Desel C, Hosein F (2009) ADP-glucose pyrophosphorylase-deficient pea embryos reveal specific transcriptional and metabolic changes of carbon-nitrogen metabolism and stress responses. Plant Physiol 149:395–411

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wen L, Liu G, Li SQ, Wan CX, Tao J, Xu KY, Zhang ZJ, Zhu YG (2007) Proteomic analysis of anthers from Honglian cytoplasmic male sterility line rice and its corresponding maintainer and hybrid. Bot Stud 48:293–309

    CAS  Google Scholar 

  • Xiao X, Yang Y, Yang Y, Lin J, Tang D, Liu X (2009) Comparative analysis of young panicle proteome in thermo-sensitive genic male-sterile rice Zhu-1S under sterile and fertile conditions. Biotechnol Lett 31:157–161

    Article  CAS  PubMed  Google Scholar 

  • Yan JX, Wait R, Berkelman T, Harry RA, Westbrook JA, Wheeler CH, Dunn MJ (2000) A modified silver staining protocol for visualization of proteins compatible with matrix-assisted laser desorption/ionization and electrospray ionization-mass spectrometry. Electrophoresis 21:3666–3672

    Article  CAS  PubMed  Google Scholar 

  • Yue J, Ren Y, Wu S, Zhang X, Wang H, Tang C (2014) Differential proteomic studies of the genic male-sterile line and fertile line anthers of upland cotton (Gossypium hirsutum L.). Genes Genom:1–12 doi: 10.1007/s13258-014-0176-y

  • Zhang H, Xu C, He Y, Zong J, Yang X, Si H, Sun Z, Hu J, Liang W, Zhang D (2013) Mutation in CSA creates a new photoperiod-sensitive genic male sterile line applicable for hybrid rice seed production. Proc Natl Acad Sci 110:76–81

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhang PB, Ding JH, Zhang QF (2010) The leaves and sites for inducing fertility change by photoperiod in photoperiod-sensitive genic male sterile rice. Mol Plant Breed 8:641–646

    Google Scholar 

  • Zheng R, Yue SJ, Xu XY, Liu JY, Xu Q, Wang XL, Han L, Yu DY (2012) Proteome analysis of the wild and YX-1 male sterile mutant anthers of wolfberry (Lycium barbarum L.). PLoS ONE 7:e41861

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhou H, Liu QJ, Li J, Jiang DG, Zhou LY, Wu P, Lu S, Li F, Zhu LY, Liu ZL (2012) Photoperiod-and thermo-sensitive genic male sterility in rice are caused by a point mutation in a novel noncoding RNA that produces a small RNA. Cell Res 22:649–660

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (Grant No. 31371600).

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The authors have declared no conflict of interest.

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Correspondence to Hanlai Zeng.

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Supplementary Fig. S1

The experimental design of this study. (TIFF 4,960 kb)

Supplementary Fig. S2

Close-up views of the regions showing the distribution of some differentially accumulated protein spots. In each panel, protein patterns of D52S under SD (left) and LD (middle) conditions are shown. Differentially accumulated protein spots are indicated by black arrows. The quantitative analysis of each protein spot is presented in the right column. The data are the mean values ±SEM (n = 3). (TIFF 3,403 kb)

Supplementary Fig. S3

The category distribution of the identified protein spots from young panicles, leaf sheaths and leaves analysed by WEGO. (TIFF 913 kb)

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Supplementary material 5 (PDF 3,403 kb)

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Chen, Z., Li, H., Ma, X. et al. Proteome alterations of reverse photoperiod-sensitive genic male sterile rice (Oryza sativa L.) at fertility transformation stage. Genes Genom 36, 711–726 (2014). https://doi.org/10.1007/s13258-014-0205-x

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