Differentially Expressed Genes Shared by Two Distinct Cytoplasmic Male Sterility (CMS) Types of Silene vulgaris Suggest the Importance of Oxidative Stress in Pollen Abortion

. 2020 Dec 16 ; 9 (12) : . [epub] 20201216

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid33339225

Cytoplasmic male sterility (CMS), encoded by the interacting mitochondrial and nuclear genes, causes pollen abortion or non-viability. CMS is widely used in agriculture and extensively studied in crops. Much less is known about CMS in wild species. We performed a comparative transcriptomic analysis of male sterile and fertile individuals of Silene vulgaris, a model plant for the study of gynodioecy, to reveal the genes responsible for pollen abortion in this species. We used RNA-seq datasets previously employed for the analysis of mitochondrial and plastid transcriptomes of female and hermaphrodite flower buds, making it possible to compare the transcriptomes derived from three genomes in the same RNA specimen. We assembled de novo transcriptomes for two haplotypes of S. vulgaris and identified differentially expressed genes between the females and hermaphrodites, associated with stress response or pollen development. The gene for alternative oxidase was downregulated in females. The genetic pathways controlling CMS in S. vulgaris are similar to those in crops. The high number of the differentially expressed nuclear genes contrasts with the uniformity of organellar transcriptomes across genders, which suggests these pathways are evolutionarily conserved and that selective mechanisms may shield organellar transcription against changes in the cytoplasmic transcriptome.

Zobrazit více v PubMed

Horn R., Gupta K.J., Colombo N. Mitochondrion role in molecular basis of cytoplasmic male sterility. Mitochondrion. 2014;19:198–205. doi: 10.1016/j.mito.2014.04.004. PubMed DOI

Touzet P., Meyer E.H. Cytoplasmic male sterility and mitochondrial metabolism in plants. Mitochondrion. 2014;19:166–171. doi: 10.1016/j.mito.2014.04.009. PubMed DOI

Hanson M.R. Interactions of Mitochondrial and Nuclear Genes That Affect Male Gametophyte Development. Plant Cell. 2004;16:S154–S169. doi: 10.1105/tpc.015966. PubMed DOI PMC

Olson M.S., McCauley D.E. Mitochondrial DNA diversity, population structure, and gender association in the gynodioecious plant Silene vulgaris. Evolution. 2002;56:253–262. doi: 10.1111/j.0014-3820.2002.tb01335.x. PubMed DOI

Dufay M., Champelovier P., Käfer J., Henry J.P., Mousset S., Ab Marais G. An angiosperm-wide analysis of the gynodioecy–dioecy pathway. Ann. Bot. 2014;114:539–548. doi: 10.1093/aob/mcu134. PubMed DOI PMC

Renner S.S. The relative and absolute frequencies of angiosperm sexual systems: Dioecy, monoecy, gynodioecy, and an updated online database. Am. J. Bot. 2014;101:1588–1596. doi: 10.3732/ajb.1400196. PubMed DOI

Bernasconi G., Antonovics J., Biere A.L., Charlesworth D., Delph L.F., Filatov D.A., Giraud T., Hood M.E., Marais G.A.B., McCauley D.W., et al. Silene as a model system in ecology and evolution. Heredity. 2009;103:5–14. doi: 10.1038/hdy.2009.34. PubMed DOI

Štorchová H., Olson M.S. Comparison between mitochondrial and chloroplast DNA variation in the native range of Silene vulgaris. Mol. Ecol. 2004;13:2909–2919. doi: 10.1111/j.1365-294X.2004.02278.x. PubMed DOI

Barr C.M., Keller S.R., Ingvarsson P., Sloan D.B., Taylor U.R. Variation in Mutation Rate and Polymorphism Among Mitochondrial Genes of Silene vulgaris. Mol. Biol. Evol. 2007;24:1783–1791. doi: 10.1093/molbev/msm106. PubMed DOI

Sebasky M.E., Keller S.R., Taylor D.R. Investigating past range dynamics for a weed of cultivation, Silene vulgaris. Ecol. Evol. 2016;6:4800–4811. doi: 10.1002/ece3.2250. PubMed DOI PMC

Štorchová H., Müller K., Lau S., Olson M.S. Mosaic Origins of a Complex Chimeric Mitochondrial Gene in Silene vulgaris. PLoS ONE. 2012;7:e30401. doi: 10.1371/journal.pone.0030401. PubMed DOI PMC

Štorchová H., Stone J.D., Sloan D.B., Abeyawardana O.A.J., Müller K., Walterová J., Pažoutová M. Homologous recombination changes the context of Cytochrome b transcription in the mitochondrial genome of Silene vulgaris KRA. BMC Genom. 2018;19:874. doi: 10.1186/s12864-018-5254-0. PubMed DOI PMC

Sloan D.B., Müller K., McCauley D.E., Taylor D.R., Štorchová H. Intraspecific variation in mitochondrial genome sequence, structure, and gene content inSilene vulgaris, an angiosperm with pervasive cytoplasmic male sterility. New Phytol. 2012;196:1228–1239. doi: 10.1111/j.1469-8137.2012.04340.x. PubMed DOI

Xie Y., Zhang W., Wang Y., Xu L., Zhu X., Muleke E.M., Liu L. Comprehensive transcriptome-based characterization of differentially expressed genes involved in microsporogenesis of radish CMS line and its maintainer. Funct. Integr. Genom. 2016;16:529–543. doi: 10.1007/s10142-016-0504-1. PubMed DOI

Li C., Zhao Z., Liu Y., Liang B., Guan S., Lan H., Wang J., Lu Y., Cao M. Comparative transcriptome analysis of isonuclear-alloplasmic lines unmask key transcription factor genes and metabolic pathways involved in sterility of maize CMS-C. PeerJ. 2017;5:e3408. doi: 10.7717/peerj.3408. PubMed DOI PMC

Pei X., Jing Z., Tang Z., Zhu Y. Comparative transcriptome analysis provides insight into differentially expressed genes related to cytoplasmic male sterility in broccoli (Brassica oleracea var. italica) Sci. Hortic. 2017;217:234–242. doi: 10.1016/j.scienta.2017.01.041. DOI

Chen G., Ye X., Zhang S., Zhu S., Yuan L., Hou J., Wang C. Comparative Transcriptome Analysis between Fertile and CMS Flower Buds in Wucai (Brassica campestris L.) BMC Genom. 2018;19:908. doi: 10.1186/s12864-018-5331-4. PubMed DOI PMC

Hamid R., Tomar R.S., Marashi H., Shafaroudi S.M., Golakiya B., Mohsenpour M. Transcriptome profiling and cataloging differential gene expression in floral buds of fertile and sterile lines of cotton (Gossypium hirsutum L.) Gene. 2018;660:80–91. doi: 10.1016/j.gene.2018.03.070. PubMed DOI

Liu B., Ou C., Chen S., Cao Q., Zhao Z., Miao Z., Kong X., Zhuang F.-Y. Differentially Expressed Genes between Carrot Petaloid Cytoplasmic Male Sterile and Maintainer during Floral Development. Sci. Rep. 2019;9:17384. doi: 10.1038/s41598-019-53717-x. PubMed DOI PMC

Janzen G.M., Wang L., Hufford M.B. The extent of adaptive wild introgression in crops. New Phytol. 2018;221:1279–1288. doi: 10.1111/nph.15457. PubMed DOI

Haas M., Himmelbach A., Mascher M. The contribution of cis- and trans-acting variants to gene regulation in wild and domesticated barley under cold stress and control conditions. J. Exp. Bot. 2020;71:2573–2584. doi: 10.1093/jxb/eraa036. PubMed DOI PMC

Case A.L., Willis J.H. Hybrid male sterility in Mimulus (Phrymaceae) is associated with a geographically restricted mitochondrial rearrangeMENT. Evolution. 2008;62:1026–1039. doi: 10.1111/j.1558-5646.2008.00360.x. PubMed DOI

Yamamoto M.P., Shinada H., Onodera Y., Komaki C., Mikami T., Kubo T. A male sterility-associated mitochondrial protein in wild beets causes pollen disruption in transgenic plants. Plant J. 2008;54:1027–1036. doi: 10.1111/j.1365-313X.2008.03473.x. PubMed DOI

Stone J.D., Koloušková P., Sloan D.B., Štorchová H. Non-coding RNA may be associated with cytoplasmic male sterility in Silene vulgaris. J. Exp. Bot. 2017;68:1599–1612. doi: 10.1093/jxb/erx057. PubMed DOI PMC

Krüger M., Abeyawardana O.A.J., Juříček M., Krüger C., Štorchová H. Variation in plastid genomes in the gynodioecious species Silene vulgaris. BMC Plant Biol. 2019;19:568. doi: 10.1186/s12870-019-2193-0. PubMed DOI PMC

Song L., Florea L. Rcorrector: Efficient and accurate error correction for Illumina RNA-seq reads. GigaScience. 2015;4:48. doi: 10.1186/s13742-015-0089-y. PubMed DOI PMC

Kopylova E., Noé L., Touzet H. SortMeRNA: Fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics. 2012;28:3211–3217. doi: 10.1093/bioinformatics/bts611. PubMed DOI

Grabherr M.G., Haas B.J., Yassour M., Levin J.Z., Thompson D.A., Amit I., Adiconis X., Fan L., Raychowdhury R., Zeng Q., et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 2011;29:644–652. doi: 10.1038/nbt.1883. PubMed DOI PMC

Li W., Godzik A. Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22:1658–1659. doi: 10.1093/bioinformatics/btl158. PubMed DOI

Gilbert D.G. Longest protein, longest transcript or most expression, for accurate gene reconstruction of transcriptomes? bioRxiv. 2019:829184. doi: 10.1101/829184. DOI

Seppey M., Manni M., Zdobnov E.M. BUSCO: Assessing genome assembly and annotation completeness. In: Kollmar M., editor. Gene Prediction. Volume 1962. Methods in Molecular Biology; Humana; New York, NY, USA: 2019. pp. 227–245. PubMed

Li B., Fillmore N., Bai Y., Collins M., Thomson J.A., Stewart R., Dewey C.N. Evaluation of de novo transcriptome assemblies from RNA-Seq data. Genome Biol. 2014;15:553. doi: 10.1186/s13059-014-0553-5. PubMed DOI PMC

Zhang J., Ruhlman T., Mower J.P., Jansen R. Comparative analyses of two Geraniaceae transcriptomes using next-generation sequencing. BMC Plant Biol. 2013;13:228. doi: 10.1186/1471-2229-13-228. PubMed DOI PMC

Haas B.J., Papanicolaou A., Yassour M., Grabherr M., Blood P.D., Bowden J., Couger M.B., Eccles D., Li B., Lieber M., et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 2013;8:1494–1512. doi: 10.1038/nprot.2013.084. PubMed DOI PMC

Li B., Dewey C.N. RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform. 2011;12:323. doi: 10.1186/1471-2105-12-323. PubMed DOI PMC

Langmead B., Salzberg S.L. Fast gapped-read alignment with Bowtie 2. Nat. Methods. 2012;9:357–359. doi: 10.1038/nmeth.1923. PubMed DOI PMC

Patro R., Duggal G., Love M.I., Irizarry M.I.L.R.A., Kingsford C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods. 2017;14:417–419. doi: 10.1038/nmeth.4197. PubMed DOI PMC

Love M.I., Huber W., Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550. doi: 10.1186/s13059-014-0550-8. PubMed DOI PMC

Robinson M.D., Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 2010;11:R25. doi: 10.1186/gb-2010-11-3-r25. PubMed DOI PMC

Koloušková P., Stone J.D., Štorchová H. Evaluation of reference genes for reverse transcription quantitative real-time PCR (RT-qPCR) studies in Silene vulgaris considering the method of cDNA preparation. PLoS ONE. 2017;12:e0183470. doi: 10.1371/journal.pone.0183470. PubMed DOI PMC

Stone J.D., Štorchová H. The application of RNA-seq to the comprehensive analysis of plant mitochondrial transcriptomes. Mol. Genet. Genom. 2014;290:1–9. doi: 10.1007/s00438-014-0905-6. PubMed DOI

Sloan D.B., Keller S.R., Berardi A.E., Sanderson B.J., Karpovich J.F., Taylor D.R. De novo transcriptome assembly and polymorphism detection in the flowering plant Silene vulgaris (Caryophyllaceae) Mol. Ecol. Resour. 2011;12:333–343. doi: 10.1111/j.1755-0998.2011.03079.x. PubMed DOI

Gastaldi V., Lucero L., Ferrero L., Ariel F., Gonzalez D.H. Class-I TCP Transcription Factors Activate the SAUR63 Gene Subfamily in Gibberellin-Dependent Stamen Filament Elongation. Plant Physiol. 2020;182:2096–2110. doi: 10.1104/pp.19.01501. PubMed DOI PMC

Verma N. Transcriptional regulation of anther development in Arabidopsis. Gene. 2019;689:202–209. doi: 10.1016/j.gene.2018.12.022. PubMed DOI

Hu L., Liang W., Yin C., Cui X., Zong J., Wang X., Hu J., Zhang D. Rice MADS3 Regulates ROS Homeostasis during Late Anther Development. Plant Cell. 2011;23:515–533. doi: 10.1105/tpc.110.074369. PubMed DOI PMC

Routray P., Li T., Yamasaki A., Yoshinari A., Takano J., Choi W.G., Sams C.E., Roberts D.M. Nodulin Intrinsic Protein 7;1 Is a Tapetal Boric Acid Channel Involved in Pollen Cell Wall Formation. Plant Physiol. 2018;178:1269–1283. doi: 10.1104/pp.18.00604. PubMed DOI PMC

Cecchetti V., Brunetti P., Napoli N., Fattorini L., Altamura M.M., Costantino P., Cardarelli M. ABCB1 and ABCB19 auxin transporters have synergistic effects on early and lateArabidopsisanther development. J. Integr. Plant Biol. 2015;57:1089–1098. doi: 10.1111/jipb.12332. PubMed DOI

Sheng Y., Wang Y., Jiao S., Jin Y., Ji P., Luan F. Mapping and Preliminary Analysis of ABORTED MICROSPORES (AMS) as the Candidate Gene Underlying the Male Sterility (MS-5) Mutant in Melon (Cucumis melo L.) Front. Plant Sci. 2017;8:902. doi: 10.3389/fpls.2017.00902. PubMed DOI PMC

Zluvova J., Zak J., Janousek B., Vyskot B. Dioecious Silene latifolia plants show sexual dimorphism in the vegetative stage. BMC Plant Biol. 2010;10:208. doi: 10.1186/1471-2229-10-208. PubMed DOI PMC

Dobritsa A.A., Geanconteri A., Shrestha J., Carlson A.L., Kooyers N., Coerper D., Urbanczyk-Wochniak E., Bench B.J., Sumner L.W., Swanson R., et al. A Large-Scale Genetic Screen in Arabidopsis to Identify Genes Involved in Pollen Exine Production. Plant Physiol. 2011;157:947–970. doi: 10.1104/pp.111.179523. PubMed DOI PMC

Jiang J., Zhang Z., Cao J. Pollen wall development: The associated enzymes and metabolic pathways. Plant Biol. 2012;15:249–263. doi: 10.1111/j.1438-8677.2012.00706.x. PubMed DOI

Bosch M., Hepler P.K. Pectin Methylesterases and Pectin Dynamics in Pollen Tubes. Plant Cell. 2005;17:3219–3226. doi: 10.1105/tpc.105.037473. PubMed DOI PMC

Yuan Q., Song C., Gao L., Zhang H., Yang C., Sheng J., Ren J., Chen D., Wang Y. Transcriptome de novo assembly and analysis of differentially expressed genes related to cytoplasmic male sterility in onion. Plant Physiol. Biochem. 2018;125:35–44. doi: 10.1016/j.plaphy.2018.01.015. PubMed DOI

Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 2002;7:405–410. doi: 10.1016/S1360-1385(02)02312-9. PubMed DOI

Yang L., Wu Y., Zhang M., Zhang J., Stewart J.M., Xing C., Wu J., Jin S. Transcriptome, cytological and biochemical analysis of cytoplasmic male sterility and maintainer line in CMS-D8 cotton. Plant Mol. Biol. 2018;97:537–551. doi: 10.1007/s11103-018-0757-2. PubMed DOI

Luo D., Xu H., Liu Z., Guo J., Li H., Chen L., Fang C., Zhang Q., Bai M., Yao N., et al. A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nat. Genet. 2013;45:573–577. doi: 10.1038/ng.2570. PubMed DOI

Yi J., Moon S., Lee Y.-S., Zhu L., Liang W., Zhang D., Jung K.-H., An G. Defective Tapetum Cell Death 1 (DTC1) Regulates ROS Levels by Binding to Metallothionein during Tapetum Degeneration. Plant Physiol. 2016;170:1611–1623. doi: 10.1104/pp.15.01561. PubMed DOI PMC

Escamez S., Stael S., Vainonen J.P., Willems P., Jin H., Kimura S., Van Breusegem F., Gevaert K., Wrzaczek M., Tuominen H. Extracellular peptide Kratos restricts cell death during vascular development and stress in Arabidopsis. J. Exp. Bot. 2019;70:2199–2210. doi: 10.1093/jxb/erz021. PubMed DOI PMC

Qin T., Tian Q., Wang G., Xiong L. LOWER TEMPERATURE 1 Enhances ABA Responses and Plant Drought Tolerance by Modulating the Stability and Localization of C2-Domain ABA-Related Proteins in Arabidopsis. Mol. Plant. 2019;12:1243–1258. doi: 10.1016/j.molp.2019.05.002. PubMed DOI

Ding B., Hao M., Mei D., Zaman Q.U., Sang S.-F., Wang H., Wang W.-X., Fu L., Cheng H., Hu Q. Transcriptome and Hormone Comparison of Three Cytoplasmic Male Sterile Systems in Brassica napus. Int. J. Mol. Sci. 2018;19:4022. doi: 10.3390/ijms19124022. PubMed DOI PMC

Ilyas M., Rasheed A., Mahmood T. Functional characterization of germin and germin-like protein genes in various plant species using transgenic approaches. Biotechnol. Lett. 2016;38:1405–1421. doi: 10.1007/s10529-016-2129-9. PubMed DOI

Millar A.H., Whelan J., Soole K.L., Day D.A. Organization and Regulation of Mitochondrial Respiration in Plants. Annu. Rev. Plant Biol. 2011;62:79–104. doi: 10.1146/annurev-arplant-042110-103857. PubMed DOI

Schwarzländer M., König A.-C., Sweetlove L.J., Finkemeier I. The impact of impaired mitochondrial function on retrograde signalling: A meta-analysis of transcriptomic responses. J. Exp. Bot. 2011;63:1735–1750. doi: 10.1093/jxb/err374. PubMed DOI

Kühn K., Obata T., Feher K., Bock R., Fernie A.R., Meyer E.H. Complete Mitochondrial Complex I Deficiency Induces an Up-Regulation of Respiratory Fluxes That Is Abolished by Traces of Functional Complex I. Plant Physiol. 2015;168:1537–1549. doi: 10.1104/pp.15.00589. PubMed DOI PMC

Merendino L., Courtois F., Grübler B., Bastien O., Straetmanns V., Chevalier F., Lerbs-Mache S., Lurin C., Pfannschmidt T. Retrograde signals from mitochondria reprogramme skoto-morphogenesis in Arabidopsis thaliana via alternative oxidase 1a. Philos. Trans. R. Soc. B Biol. Sci. 2020;375:20190567. doi: 10.1098/rstb.2019.0567. PubMed DOI PMC

Suzuki H., Rodriguez-Uribe L., Xu J., Zhang J. Transcriptome analysis of cytoplasmic male sterility and restoration in CMS-D8 cotton. Plant Cell Rep. 2013;32:1531–1542. doi: 10.1007/s00299-013-1465-7. PubMed DOI

Niazi A.K., Delannoy E., Iqbal R.K., Mileshina D., Val R., Gabryelska M., Wyszko E., Taconnat L., Szymanski M., Barciszewski J., et al. Mitochondrial Transcriptome Control and Intercompartment Cross-Talk During Plant Development. Cells. 2019;8:583. doi: 10.3390/cells8060583. PubMed DOI PMC

Zheng B.-B., Wu X.-M., Ge X.-X., Deng X.-X., Grosser J.W., Guo W.-W. Comparative Transcript Profiling of a Male Sterile Cybrid Pummelo and Its Fertile Type Revealed Altered Gene Expression Related to Flower Development. PLoS ONE. 2012;7:e43758. doi: 10.1371/journal.pone.0043758. PubMed DOI PMC

Hamid R., Jacob F., Marashi H., Rathod V., Tomar R.S. Uncloaking lncRNA-meditated gene expression as a potential regulator of CMS in cotton (Gossypium hirsutum L.) Genomics. 2020;112:3354–3364. doi: 10.1016/j.ygeno.2020.06.027. PubMed DOI

Colombatti F., Gonzalez D.H., Welchen E. Plant mitochondria under pathogen attack: A sigh of relief or a last breath? Mitochondrion. 2014;19:238–244. doi: 10.1016/j.mito.2014.03.006. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace