Abstract
Main conclusion
Bioinformatic analysis identified the function of genes regulating wheat fertility. Barley stripe mosaic virus-induced gene silencing verified that the genes TaMut11 and TaSF3 are involved in pollen development and related to fertility conversion.
Abstract
Environment-sensitive genic male sterility is of vital importance to hybrid vigor in crop production and breeding. Therefore, it is meaningful to study the function of the genes related to pollen development and male sterility, which is still not fully understand currently. In this study, YanZhan 4110S, a new thermo-sensitive genic male sterility wheat line, and its near-isogenic line YanZhan 4110 were analyzed. Through comparative transcriptome basic bioinformatics and weighted gene co-expression network to further identify some hub genes, the genes TaMut11 and TaSF3 associated with pollen development and male sterility induced by high-temperature were identified in YanZhan 4110S. Further verification through barley stripe mosaic virus-induced gene silencing elucidated that the silencing of TaMut11 and TaSF3 caused pollen abortion, finally resulting in the declination of fertility. These findings provided data on the abortive mechanism in environment-sensitive genic male sterility wheat.
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Data availability
All of datasets supporting the conclusions of this article are available in NCBI Sequence Read Archive under accession SRA: SRP211924.
Abbreviations
- Bn/Tn:
-
Binucleate/trinucleate stage
- BSMV:
-
Barley stripe mosaic virus
- DEGs:
-
Differentially expressed genes
- Lun:
-
Late uninucleate stage
- VIGS:
-
Virus-induced gene silencing
- VS:
-
Versus
- WGCNA:
-
Weighted Gene Co-Expression Network Analysis
References
Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402. https://doi.org/10.1093/nar/25.17.3389
Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106. https://doi.org/10.1186/gb-2010-11-10-r106
Boavida LC, Becker JD, Feijo JA (2005) The making of gametes in higher plants. Int J Dev Biol 49(5–6):595–614. https://doi.org/10.1387/ijdb.052019lb
Cakir C, Scofield SR (2008) Evaluating the ability of the barley stripe mosaic virus-induced gene silencing system to simultaneously silence two wheat genes. Cereal Res Commun 36:217–222. https://doi.org/10.1556/CRC.36.2008.Suppl.B.18
Cakir C, Tor M (2010) Factors influencing barley stripe mosaic virus-mediated gene silencing in wheat. Physiol Mol Plant Pathol 74(3–4):246–253. https://doi.org/10.1016/j.pmpp.2010.04.001
Chen HM, Pan XM (2001) Tropical and subtropical hybrid maize breeding and its utilization of heterosis. Seed 2:57–58. https://doi.org/10.16590/j.cnki.1001-4705.2001.02.069
Chen L, Shahid MQ, Wu JW, Chen ZX, Wang L, Liu XD (2018) Cytological and transcriptome analyses reveal abrupt gene expression for meiosis and saccharide metabolisms that associated with pollen abortion in autotetraploid rice. Mol Genet Genomics 293(6):1407–1420. https://doi.org/10.1007/s00438-018-1471-0
Cheng YF, Wang Q, Li ZJ, Cui JM, Hu SW, Zhao HX, Chen MS (2013) Cytological and comparative proteomic analyses on male sterility in Brassica napus L. induced by the chemical hybridization agent monosulphuron ester sodium. PLoS One 8(11):e80191. https://doi.org/10.1371/journal.pone.0080191
Constantin GD, Krath BN, MacFarlane SA, Nicolaisen M, Johansen IE, Lund OS (2004) Virus-induced gene silencing as a tool for functional genomics in a legume species. Plant J 40(4):622–631. https://doi.org/10.1111/j.1365-313X.2004.02233.x
Darwin C (2009) The effects of cross and self-fertilisation in the vegetable kingdom. Camb Univ Press 15:329–332. https://doi.org/10.1387/ijdb.052019lb
Delventhal R, Falter C, Strugala R, Zellerhoff N, Schaffrath U (2014) Ectoparasitic growth of Magnaporthe on barley triggers expression of the putative barley wax biosynthesis gene CYP96B22 which is involved in penetration resistance. BMC Plant Biol 14:26. https://doi.org/10.1186/1471-2229-14-26
Deng HF, Qiang HE (2017) Research and prospects of hybrid rice with strong heterosis in China. Sci Technol Rev 35(10):32–37. https://doi.org/10.3981/j.issn.1000-7857.2017.10.004
Djebali S, Davis CA, Merkel A et al (2012) Landscape of transcription in human cells. Nature 489(7414):101–108. https://doi.org/10.1038/nature11233
Duan XY, Wang XJ, Fu YP, Tang CL, Li XR, Cheng YL, Feng H, Huang LL, Kang ZS (2013) TaEIL1, a wheat homologue of AtEIN3, acts as a negative regulator in the wheat-stripe rust fungus interaction. Mol Plant Pathol 14(7):728–739. https://doi.org/10.1111/mpp.12044
Fu DQ, Zhu BZ, Zhu HL, Jiang WB, Luo YB (2005) Virus-induced gene silencing in tomato fruit. Plant J 43(2):299–308. https://doi.org/10.1111/j.1365-313X.2005.02441.x
Gao FM, Ma DY, Yin GH, Rasheed A, Dong Y, Xiao YG, Xia XC, Wu XX, He ZH (2017) Genetic progress in grain yield and physiological traits in Chinese wheat cultivars of southern yellow and Huai valley winter wheat zone since 1950. Crop Sci 57(2):760–773. https://doi.org/10.2135/cropsci2016.05.0362
George GM, van der Merwe MJ, Nunes-Nesi A, Bauer R, Fernie AR, Kossmann J, Lloyd JR (2010) Virus-induced gene silencing of plastidial soluble inorganic pyrophosphatase impairs essential leaf anabolic pathways and reduces drought stress tolerance in Nicotiana benthamiana. Plant Physiol 154(1):55–66. https://doi.org/10.1104/pp.110.157776
Holzberg S, Brosio P, Gross C, Pogue GP (2002) Barley stripe mosaic virus-induced gene silencing in a monocot plant. Plant J 30(3):315–327. https://doi.org/10.1046/j.1365-313x.2002.01291.x
Ishiguro S, Ogasawara K, Fujino K, Sato Y, Kishima Y (2014) Low temperature-responsive changes in the anther transcriptome’s repeat sequences are indicative of stress sensitivity and pollen sterility in rice strains. Plant Physiol 164(2):671–682. https://doi.org/10.1104/pp.113.230656
Jackson AO, Lim HS, Bragg J, Ganesan U, Lee MY (2009) Hordeivirus replication, movement, and pathogenesis. Annu Rev Phytopathol 47:385–422. https://doi.org/10.1146/annurev-phyto-080508-081733
Jiao J, Wang YC, Selvaraj JN, Xing FG, Liu Y (2015) Barley Stripe Mosaic Virus (BSMV) induced microRNA silencing in common wheat (Triticum aestivum L.). PLoS One 10(5):e0126621. https://doi.org/10.1371/journal.pone.0126621
Kang GZ, Li GZ, Ma HZ, Wang CY, Guo TC (2013) Proteomic analysis on the leaves of TaBTF3 gene virus-induced silenced wheat plants may reveal its regulatory mechanism. J Proteomics 83:130–143. https://doi.org/10.1016/j.jprot.2013.03.020
Kim D, Landmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12(4):357-U121. https://doi.org/10.1038/Nmeth.3317
Kumar S, Jordan MC, Datla R, Cloutier S (2013) The LuWD40–1 gene encoding WD repeat protein regulates growth and pollen viability in flax (Linum Usitatissimum L.). PLoS One 8(7):e69124. https://doi.org/10.1371/journal.pone.0069124
Lacomme C, Hrubikova K, Hein I (2003) Enhancement of virus-induced gene silencing through viral-based production of inverted-repeats. Plant J 34(4):543–553. https://doi.org/10.1046/j.1365-313X.2003.01733.x
Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9:559. https://doi.org/10.1186/1471-2105-9-559
Lasa JM (1993) Male sterility. Plant Breeding 30(43):213–228. https://doi.org/10.1007/978-94-011-1524-7_15
Lee WS, Kanyuka HK (2012) Barley stripe mosaic virus-mediated tools for investigating gene function in cereal plants and their pathogens: virus-induced gene silencing, host-mediated gene silencing, and virus-mediated overexpression of heterologous protein. Plant Physiol 160(2):582–590. https://doi.org/10.1104/pp.112.203489
Li JJ, Han SH, Ding XL, He TT, Dai JY, Yang SP, Gai JY (2015) Comparative transcriptome analysis between the cytoplasmic male sterile line NJCMS1A and its maintainer NJCMS1B in soybean (Glycine max (L.) Merr). PLoS One 10(5):e0126771. https://doi.org/10.1371/journal.pone.0126771
Li JJ, Ding XL, Han SH, He TT, Zhang H, Yang LS, Yang SP, Gai JY (2016) Differential proteomics analysis to identify proteins and pathways associated with male sterility of soybean using iTRAQ-based strategy. J Proteomics 138:72–82. https://doi.org/10.1016/j.jprot.2016.02.017
Liu ZJ (1993) The analysis of causes and groups of plant male sterility. J Sichuan Teach Coll 14:296–305. https://doi.org/10.4028/www.scientific.net/AMR.610-613.1513
Liu YM, Zhang L, Qiu T, Zhao ZF, Cao MJ (2016) Research progress on mechanisms of male sterility in plants based on high-throughput RNA sequencing. Hereditas 38:677–687. https://doi.org/10.16288/j.yczz.16-031
Liu ZH, Li S, Li W, Liu Q, Zhang LL, Song XY (2020) Comparative transcriptome analysis indicates that a core transcriptional network mediates isonuclear alloplasmic male sterility in wheat (Triticum aestivum L.). BMC Plant Biol 20:10. https://doi.org/10.1186/s12870-019-2196-x
Mantelin S, Peng HC, Li BB, Atamian HS, Takken FLW, Kaloshian I (2011) The receptor-like kinase SlSERK1 is required for Mi-1-mediated resistance to potato aphids in tomato. Plant J 67(3):459–471. https://doi.org/10.1111/j.1365-313X.2011.04609.x
Panwar V, McCallum B, Bakkeren G (2013) Host-induced gene silencing of wheat leaf rust fungus Puccinia triticina pathogenicity genes mediated by the barley stripe mosaic virus. Plant Mol Biol 81(6):595–608. https://doi.org/10.1007/s11103-013-0022-7
Pertea M, Pertea GM, Antonescu CM, Chang TC, Mendell JT, Salzberg SL (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33(3):290–295. https://doi.org/10.1038/nbt.3122
Ramegowda V, Mysore KS, Senthil-Kumar M (2014) Virus-induced gene silencing is a versatile tool for unraveling the functional relevance of multiple abiotic-stress-responsive genes in crop plants. Front Plant Sci 5:323. https://doi.org/10.3389/fpls.2014.00323
Ray DK, Mueller ND, West PC, Foley JA (2013) Yield trends are insufficient to double global crop production by 2050. PLoS One 8(6):e66428. https://doi.org/10.1371/journal.pone.0066428
Schulze SK, Kanwar R, Golzenleuchter M, Therneau TM, Beutler AS (2012) SERE: Single-parameter quality control and sample comparison for RNA-Seq. BMC Genomics 13:524. https://doi.org/10.1186/1471-2164-13-524
Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of MicroRNAs on the plant transcriptome. Dev Cell 8(4):517–527. https://doi.org/10.1016/j.devcel.2005.01.018
Scofield SR, Huang L, Brandt AS, Gill BS (2005) Development of a virus-induced gene-silencing system for hexaploid wheat and its use in functional analysis of the Lr21-mediated leaf rust resistance pathway. Plant Physiol 138(4):2165–2173. https://doi.org/10.1104/pp.105.061861
Singh SP, Srivastava R, Kumar J (2015) Male sterility systems in wheat and opportunities for hybrid wheat development. Acta Physiol Plant 37:1713. https://doi.org/10.1007/S11738-014-1713-7
Valentine T, Shaw J, Blok VC, Phillips MS, Oparka KJ, Lacomme C (2004) Efficient virus-induced gene silencing in roots using a modified tobacco rattle virus vector. Plant Physiol 136(4):3999–4009. https://doi.org/10.1104/pp.104.051466
Wang LK, Feng ZX, Wang X, Wang XW, Zhang XG (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26(1):136–138. https://doi.org/10.1093/bioinformatics/btp612
Wang S, Wang C, Zhang XX, Chen X, Liu JJ, Jia XF, Jia SQ (2016) Transcriptome de novo assembly and analysis of differentially expressed genes related to cytoplasmic male sterility in cabbage. Plant Physiol Biochem 105:224–232. https://doi.org/10.1016/j.plaphy.2016.04.027
Wei WL, Qi XQ, Wang LH, Zhang YX, Hua W, Li DH, Lv HX, Zhang XR (2011) Characterization of the sesame (Sesamum indicum L.) global transcriptome using Illumina paired-end sequencing and development of EST-SSR markers. BMC Genomics 12:451. https://doi.org/10.1186/1471-2164-12-451
Wu H, Shi N, An X, Liu C, Fu H, Cao L, Feng Y, Sun D, Zhang L (2018) Candidate genes for yellow leaf color in common wheat (Triticum aestivum L.) and major related metabolic pathways according to transcriptome profiling. Int J Mol Sci 19(6):1954. https://doi.org/10.3390/ijms19061594
Xia ZL, Su XH, Wu JY, Wu K, Zhang H (2012) Molecular cloning and functional characterization of a putative sulfite oxidase (SO) ortholog from Nicotiana benthamiana. Mol Biol Rep 39(3):2429–2437. https://doi.org/10.1007/s11033-011-0993-x
Xie CT, Wei DM, Tian HQ (2006) Advances in cell biology of male sterility in higher plants. J Plant Physiol Mol Biol 32(001):17–23. https://doi.org/10.3321/j.issn:1671-3877.2006.01.003
Xie Y, Zhang W, Wang Y, Xu L, Zhu XW, Muleke EM, Liu LW (2016) Comprehensive transcriptome-based characterization of differentially expressed genes involved in microsporogenesis of radish CMS line and its maintainer. Funct Integr Genomic 16(5):529–543. https://doi.org/10.1007/s10142-016-0504-1
Yang P (2016) Research advances on transcriptomics of plant cytoplasmic male sterility lines. Biotechnol Bull 32:1–7. https://doi.org/10.13560/j.cnki.biotech.bull.1985.2016.12.001
Yang L, Wu YL, Zhang M, Zhang JF, Stewart JM, Xing CZ, Wu JY, Jin SX (2018a) Transcriptome, cytological and biochemical analysis of cytoplasmic male sterility and maintainer line in CMS-D8 cotton. Plant Mol Biol 97(6):537–551. https://doi.org/10.1007/s11103-018-0757-2
Yang XT, Geng XX, Liu ZH, Ye JL, Xu MF, Zang LL, Song XY (2018b) A sterility induction trait in the genic male sterility wheat line 4110S induced by high temperature and its cytological response. Crop Sci 58(5):1866–1876. https://doi.org/10.2135/cropsci2017.12.0714
Yang XT, Ye JL, Zhang LL, Song XY (2020) Blocked synthesis of sporopollenin and jasmonic acid leads to pollen wall defects and anther indehiscence in genic male sterile wheat line 4110S at high temperatures. Funct Integr Genomic 20(3):383–396. https://doi.org/10.1007/s10142-019-00722-y
Ye JR, Xu ML (2012) Actin bundler PLIM2s are involved in the regulation of pollen development and tube growth in Arabidopsis. J Plant Physiol 169(5):516–522. https://doi.org/10.1016/j.jplph.2011.11.015
Zenoni S, Ferrarini A, Giacomelli E, Xumerle L, Fasoli M, Malerba G, Bellin D, Pezzotti M, Delledonne M (2010) Characterization of transcriptional complexity during berry development in Vitis vinifera using RNA-Seq. Plant Physiol 152(4):1787–1795. https://doi.org/10.1104/pp.109.149716
Zhang C, Ghabrial SA (2006) Development of Bean pod mottle virus-based vectors for stable protein expression and sequence-specific virus-induced gene silencing in soybean. Virology 344(2):401–411. https://doi.org/10.1016/j.virol.2005.08.046
Zhou HB, Li SF, Deng ZY, Wang XP, Chen T, Zhang JS, Chen SY, Ling HQ, Zhang AM, Wang DW, Zhang XQ (2007) Molecular analysis of three new receptor-like kinase genes from hexaploid wheat and evidence for their participation in the wheat hypersensitive response to stripe rust fungus infection. Plant J 52(3):420–434. https://doi.org/10.1111/j.1365-313X.2007.03246.x
Zhu XH, Pattathil S, Mazumder K, Brehm A, Hahn MG, Dinesh-Kumar SP, Joshi CP (2010) Virus-induced gene silencing offers a functional genomics platform for studying plant cell wall formation. Mol Plant 3(5):818–833. https://doi.org/10.1093/mp/ssq023
Acknowledgements
The high-throughput sequencing was financially supported by grants from the National Natural Science Foundation of China (grant number 31771874, 32072060). The funding body was not involved in the experimental design of the study, data collection, analysis and interpretation, and in writing the manuscript. The authors gratefully thank Biomarker Technologies Co., Ltd. (Beijing, China) for their help with high-throughput sequencing, and two anonymous reviewers and editors for their critical reading and invaluable comments and suggestions on the manuscript.
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Yang, X., Ye, J., Niu, F. et al. Identification and verification of genes related to pollen development and male sterility induced by high temperature in the thermo-sensitive genic male sterile wheat line. Planta 253, 83 (2021). https://doi.org/10.1007/s00425-021-03601-8
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DOI: https://doi.org/10.1007/s00425-021-03601-8