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A super PPR cluster for restoring fertility revealed by genetic mapping, homocap-seq and de novo assembly in cotton

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Abstract

Key message

Rf candidate genes were related to the super D05_PPR-cluster and verified to be individually nonfunctional.

Abstract

Restorer of fertility (Rf) genes of cytoplasmic male sterility (CMS) is commonly found to be PPR (pentatricopeptide repeat) genes, which are mostly located in a cluster of PPR genes with high similarity. Here, Homocap-seq was applied to analyze PPR clusters in ‘three lines,’ and we found broad variations within the D05_PPR-cluster in a restorer line and deduced that the D05_PPR-cluster was associated with fertility restoration. Genetic mapping of Rf and Homocap-seq analysis of three genotypes in the F2 population validated that the D05_PPR-cluster was the origin of Rf. Three Rf candidates were cloned that were the most actively expressed genes in the D05_PPR-cluster in the restorer line as revealed by their high-depth amplicons. However, further transgenic experiments showed that none of the candidates could restore fertility of the CMS line independently. Then, the members of the brand-new super D05_PPR-cluster in the restorer line, containing 14 full-length PPRs and at least 13 PPR homologous sequences, were identified by long-read resequencing, which validated the effectiveness of variation and expression prediction of Homocap-seq. Additionally, we found that several PPR duplications, including 2 of the 3 Rf candidates, had undergone site-specific selection as potentially important anther development-associated genes. Finally, we proposed that multiple PPRs were coordinately responsible for the fertility restoration of the CMS line.

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Data availability

The sequencing data of Homocap-seq and the resequencing data of PR used in this paper have been deposited under BioProject accession PRJNA701803 and PRJNA701812, respectively.

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Andolfo G, Jupe F, Witek K, Etherington GJ, Ercolano MR, Jones JDG (2014) Defining the full tomato NB-LRR resistance gene repertoire using genomic and cDNA RenSeq. BMC Plant Biol 14:120

    Article  PubMed  PubMed Central  Google Scholar 

  • Andrés-Colás N, Zhu Q, Takenaka M, De Rybel B, Weijers D, Van Der Straeten D (2017) Multiple PPR protein interactions are involved in the RNA editing system in Arabidopsis mitochondria and plastids. Proc Natl Acad Sci 114:8883–8888

    Article  PubMed  PubMed Central  Google Scholar 

  • Aronesty E (2013) Comparison of sequencing utility programs. Open Bioinform J 7:1–8

    Article  Google Scholar 

  • Arora S, Steuernagel B, Gaurav K, Chandramohan S, Long Y, Matny O, Johnson R, Enk J, Periyannan S, Singh N, Asyraf MD, Hatta M, Athiyannan N, Cheema J, Yu G, Kangara N, Ghosh S, Szabo LJ, Poland J, Bariana H, Jones JDG, Bentley AR, Ayliffe M, Olson E, Xu SS, Steffenson BJ, Lagudah E, Wulff BBH (2019) Resistance gene cloning from a wild crop relative by sequence capture and association genetics. Nat Biotechnol 37:139–143

    Article  CAS  PubMed  Google Scholar 

  • Barkan A, Small I (2014) Pentatricopeptide repeat proteins in plants. Annu Rev Plant Biol 65:415–442

    Article  CAS  PubMed  Google Scholar 

  • Brown G (1999) Unique aspects of cytoplasmic male sterility and fertility restoration in Brassica napus. J Hered 90:351–356

    Article  CAS  Google Scholar 

  • Carlsson J, Leino M, Sohlberg J, Sundström JF, Glimelius K (2008) Mitochondrial regulation of flower development. Mitochondrion 8:74–86

    Article  CAS  PubMed  Google Scholar 

  • Castandet B, Araya A (2012) The nucleocytoplasmic conflict, a driving force for the emergence of plant organellar RNA editing. IUBMB Life 64:120–125

    Article  CAS  PubMed  Google Scholar 

  • Chase CD, Gabay-Laughnan S (2004) Cytoplasmic male sterility and fertility restoration by nuclear genes. In: Daniell H, Chase C (eds) Molecular biology and biotechnology of plant organelles: chloroplasts and mitochondria. Springer, Dordrecht, pp 593–621

    Chapter  Google Scholar 

  • Chen L, Liu YG (2014) Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65:579–606

    Article  CAS  PubMed  Google Scholar 

  • Chen Z, Zhao N, Li S, Grover CE, Nie H, Wendel JF, Hua J (2017) Plant mitochondrial genome evolution and cytoplasmic male sterility. Crit Rev Plant Sci 36:1–15

    Article  CAS  Google Scholar 

  • Chen G, Zou Y, Hu J, Ding Y (2018a) Genome-wide analysis of the rice PPR gene family and their expression profiles under different stress treatments. BMC Genomics 19:720

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen S, Zhou Y, Chen Y, Gu J (2018b) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:i884–i890

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen X, Tong C, Zhang X, Song A, Hu M, Dong W, Chen F, Wang Y, Tu J, Liu S, Tang H, Zhang L (2021) A high-quality Brassica napus genome reveals expansion of transposable elements, subgenome evolution and disease resistance. Plant Biotechnol J 19:615–630

    Article  CAS  PubMed  Google Scholar 

  • Collard BCY, Mackill DJ (2008) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos Trans R Soc B Biol Sci 363:557–572

    Article  CAS  Google Scholar 

  • Dahan J, Mireau H (2013) The Rf and Rf-like PPR in higher plants, a fast-evolving subclass of PPR genes. RNA Biol 10:1469–1476

    Article  PubMed  PubMed Central  Google Scholar 

  • Dan Y, Wei L, Hua Y, King GJ, Xu F, Lei S (2017) Genome-wide identification and characterization of the aquaporin gene family and transcriptional responses to boron deficiency in Brassica napus. Front Plant Sci 8:1336

    Article  Google Scholar 

  • Eddy SR (2011) Accelerated profile HMM searches. PLoS Comp Biol 7:e1002195

    Article  CAS  Google Scholar 

  • Feng CD, Stewart JMD, Zhang JF (2005) STS markers linked to the Rf1 fertility restorer gene of cotton. Theor Appl Genet 110:237–243

    Article  CAS  PubMed  Google Scholar 

  • Feng J, Zhu H, Zhang M, Zhang X, Guo L, Qi T, Tang H, Wang H, Qiao X, Zhang B, Shahzad K, Xing C, Wu J (2020) Development and utilization of an InDel marker linked to the fertility restorer genes of CMS-D8 and CMS-D2 in cotton. Mol Biol Rep 47:1275–1282

    Article  CAS  PubMed  Google Scholar 

  • Feng J, Zhang X, Zhang M, Guo L, Qi T, Tang H, Zhu H, Wang H, Qiao X, Xing C, Wu J (2021) Physical mapping and InDel marker development for the restorer gene Rf2 in cytoplasmic male sterile CMS-D8 cotton. BMC Genomics 22:24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Francki M, Wang F, Stewart JMSM, Zhang J (2007) Molecular markers linked to the Rf2 fertility restorer gene in cotton. Genome 50:818–824

    Article  Google Scholar 

  • Fujii S, Bond CS, Small ID (2011) Selection patterns on restorer-like genes reveal a conflict between nuclear and mitochondrial genomes throughout angiosperm evolution. Proc Natl Acad Sci 108:1723–1728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaborieau L, Brown GG, Mireau H (2016) The propensity of pentatricopeptide repeat genes to evolve into restorers of cytoplasmic male sterility. Front Plant Sci 7:1816

    Article  PubMed  PubMed Central  Google Scholar 

  • Han Z, Qin Y, Li X, Yu J, Li R, Xing C, Song M, Wu J, Zhang J (2020) A genome-wide analysis of pentatricopeptide repeat (PPR) protein-encoding genes in four Gossypium species with an emphasis on their expression in floral buds, ovules, and fibers in upland cotton. Mol Genet Genom 295:55–66

    Article  CAS  Google Scholar 

  • Hanson MR, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16:S154–S169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horn R, Kusterer B, Lazarescu E, Prüfe M, Friedt W (2003) Molecular mapping of the gene restoring pollen fertility in PET1-based F1 hybrids in sunflower (Helianthus annuus L.). Theor Appl Genet 106:599–606

    Article  CAS  PubMed  Google Scholar 

  • Hu J, Fan J, Sun Z, Liu S (2019) NextPolish: a fast and efficient genome polishing tool for long-read assembly. Bioinformatics 36:2253–2255

    Article  Google Scholar 

  • Huang W, Hu J, Yu C, Huang Q, Wan L, Wang L, Qin X, Ji Y, Zhu R, Li S, Zhu Y (2012) Two non-allelic nuclear genes restore fertility in a gametophytic pattern and enhance abiotic stress tolerance in the hybrid rice plant. Theor Appl Genet 124:799–807

    Article  CAS  PubMed  Google Scholar 

  • Huang W, Yu C, Hu J, Wang L, Dan Z, Zhou W, He C, Zeng Y, Yao G, Qi J (2015) Pentatricopeptide-repeat family protein RF6 functions with hexokinase 6 to rescue rice cytoplasmic male sterility. Proc Natl Acad Sci 112:14984–14989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Igarashi K, Kazama T, Toriyama K (2016) A gene encoding pentatricopeptide repeat protein partially restores fertility in RT98-Type cytoplasmic male-sterile rice. Plant Cell Physiol 57:2187–2193

    Article  CAS  PubMed  Google Scholar 

  • IWGSC (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:eaar7191

    Article  Google Scholar 

  • Jin S, Zhang X, Nie Y, Guo X, Liang S, Zhu H (2006) Identification of a novel elite genotype for in vitro culture and genetic transformation of cotton. Biol Plant 50:519–524

    Article  CAS  Google Scholar 

  • Jo YD, Ha Y, Lee J-H, Park M, Bergsma AC, Choi H-I, Goritschnig S, Kloosterman B, van Dijk PJ, Choi D, Kang B-C (2016) Fine mapping of Restorer-of-fertility in pepper (Capsicum annuum L.) identified a candidate gene encoding a pentatricopeptide repeat (PPR)-containing protein. Theor Appl Genet 129:2003–2017

    Article  CAS  PubMed  Google Scholar 

  • Katsuo K, Mlzushima U (2008) Studies on the cytoplasmic difference among rice varieties. Oryza sativa L.: I. On the fertility of hybrids obtained reciprocally between cultivated and wild varieties. Jpn J Breed 8:1–5

    Article  Google Scholar 

  • Kolmogorov M, Yuan J, Lin Y, Pevzner PA (2019) Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol 37:540–546

    Article  CAS  PubMed  Google Scholar 

  • Kuraku S, Zmasek CM, Nishimura O, Katoh K (2013) aLeaves facilitates on-demand exploration of metazoan gene family trees on MAFFT sequence alignment server with enhanced interactivity. Nucleic Acids Res 41:W22–W28

    Article  PubMed  PubMed Central  Google Scholar 

  • Li H (2018) Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34:3094–3100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li R, Li Y, Kristiansen K, Wang J (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24:713–714

    Article  CAS  PubMed  Google Scholar 

  • Liu L, Guo W, Zhu X, Zhang T (2003) Inheritance and fine mapping of fertility restoration for cytoplasmic male sterility in Gossypium hirsutum L. Theor Appl Genet 106:461–469

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Yang Z, Wang X, Li K, An H, Liu J, Yang G, Fu T, Yi B, Hong D (2016) A mitochondria-targeted PPR protein restores pol cytoplasmic male sterility by reducing orf224 transcript levels in oilseed rape. Mol Plant 9:1082–1084

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Dong F, Wang X, Wang T, Su R, Hong D, Yang G (2017) A pentatricopeptide repeat protein restores nap cytoplasmic male sterility in Brassica napus. J Exp Bot 68:4115–4123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu S, Fadlalla T, Tang S, Li L, Ali U, Li Q, Guo L (2019) Genome-wide analysis of phospholipase D gene family and profiling of phospholipids under abiotic stresses in Brassica napus. Plant Cell Physiol 60:1556–1566

    Article  CAS  PubMed  Google Scholar 

  • Lurin C, Andrés C, Aubourg S, Bellaoui M, Bitton F, Bruyère C, Caboche M, Debast C, Gualberto J, Hoffmann B, Lecharny A, Le Ret M, Martin-Magniette M-L, Mireau H, Peeters N, Renou J-P, Szurek B, Taconnat L, Small I (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16:2089–2103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Melonek J, Zhou R, Bayer PE, Edwards D, Stein N, Small I (2019) High intraspecific diversity of Restorer-of-fertility-like genes in barley. Plant J 97:281–295

    Article  CAS  PubMed  Google Scholar 

  • Melonek J, Duarte J, Martin J, Beuf L, Murigneux A, Varenne P, Comadran J, Specel S, Levadoux S, Bernath-Levin K, Torney F, Pichon J-P, Perez P, Small I (2021) The genetic basis of cytoplasmic male sterility and fertility restoration in wheat. Nat Commun 12:1036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meyer VG (1975) Male sterility from Gossypium harknessii. J Hered 66:23–27

    Article  Google Scholar 

  • Meyer J, Pei D, Wise RP (2011) Rf8-Mediated T-urf13 transcript accumulation coincides with a pentatricopeptide repeat cluster on maize chromosome 2L. Plant Genome 4:283–299

    Article  CAS  Google Scholar 

  • Schmitz-Linneweber C, Small I (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 13:663–670

    Article  CAS  PubMed  Google Scholar 

  • Schnable PS, Wise RP (1998) The molecular basis of cytoplasmic male sterility and fertility restoration. Trends Plant Sci 3:175–180

    Article  Google Scholar 

  • Seppey M, Manni M, Zdobnov EM (2019) BUSCO: assessing genome assembly and annotation completeness. In: Kollmar M (ed) Gene prediction: methods and protocols. Springer, New York, pp 227–245

    Google Scholar 

  • Steuernagel B, Periyannan SK, Hernández-Pinzón I, Witek K, Rouse MN, Yu G, Hatta A, Ayliffe M, Bariana H, Jones JDG, Lagudah ES, Wulff BBH (2016) Rapid cloning of disease-resistance genes in plants using mutagenesis and sequence capture. Nat Biotechnol 34:652–655

    Article  CAS  PubMed  Google Scholar 

  • Steuernagel B, Witek K, Jones JDG, Wulff BBH (2017) MutRenSeq: a method for rapid cloning of plant disease resistance genes. In: Periyannan S (ed) Wheat rust diseases: methods and protocols. Springer, New York, pp 215–229

    Chapter  Google Scholar 

  • Stewart J (1992) A new cytoplasmic male sterile and restorer for cotton. In: Proceedings of the beltwide cotton conference. Memphis, National Cotton Council

  • Suzuki H, Yu J, Ness SA, O’Connell MA, Zhang J (2013) RNA editing events in mitochondrial genes by ultra-deep sequencing methods: a comparison of cytoplasmic male sterile, fertile and restored genotypes in cotton. Mol Genet Genomics 288:445–457

    Article  CAS  PubMed  Google Scholar 

  • Takenaka M, Zehrmann A, Verbitskiy D, Kugelmann M, Härtel B, Brennicke A (2012) Multiple organellar RNA editing factor (MORF) family proteins are required for RNA editing in mitochondria and plastids of plants. Proc Natl Acad Sci 109:5104–5109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tong J, Walk TC, Han P, Chen L, Shen X, Li Y, Gu C, Xie L, Hu X, Liao X, Qin L (2020) Genome-wide identification and analysis of high-affinity nitrate transporter 2 (NRT2) family genes in rapeseed (Brassica napus L.) and their responses to various stresses. BMC Plant Biol 20:464

    Article  PubMed  PubMed Central  Google Scholar 

  • Uyttewaal M, Arnal N, Quadrado M, Martin-Canadell A, Vrielynck N, Hiard S, Gherbi H, Bendahmane A, Budar F, Mireau H (2008) Characterization of Raphanus sativus pentatricopeptide repeat proteins encoded by the fertility restorer locus for Ogura cytoplasmic male sterility. Plant Cell 20:3331–3345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang F, Yue B, Hu J, Stewart JM, Zhang J (2009) A target region amplified polymorphism marker for fertility restorer gene Rf1 and chromosomal localization of Rf1 and Rf2 in cotton. Crop Sci 49:1602–1608

    Article  CAS  Google Scholar 

  • Wang M, Tu L, Yuan D, Zhu D, Shen C, Li J, Liu F, Pei L, Wang P, Zhao G, Ye Z, Huang H, Yan F, Ma Y, Zhang L, Liu M, You J, Yang Y, Liu Z, Huang F, Li B, Qiu P, Zhang Q, Zhu L, Jin S, Yang X, Min L, Li G, Chen L-L, Zheng H, Lindsey K, Lin Z, Udall JA, Zhang X (2019) Reference genome sequences of two cultivated allotetraploid cottons, Gossypium hirsutum and Gossypium barbadense. Nat Genet 51:224–229

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Xiao Q, Wei C, Chen H, Chen X, Dai C, Wen J, Ma C, Tu J, Fu T, Shen J, Yi B (2021) A mitochondria-localized pentatricopeptide repeat protein is required to restore hau cytoplasmic male sterility in Brassica napus. Theor Appl Genet 134:1377–1386

    Article  CAS  PubMed  Google Scholar 

  • Witek K, Jupe F, Witek AI, Baker D, Clark MD, Jones JDG (2016) Accelerated cloning of a potato late blight–resistance gene using RenSeq and SMRT sequencing. Nat Biotechnol 34:656–660

    Article  CAS  PubMed  Google Scholar 

  • Worstell J, Kidd H, Schertz K (1984) Relationships among male-sterility inducing cytoplasms of Sorghum. Crop Sci 24:186–189

    Article  Google Scholar 

  • Wu J, Cao X, Guo L, Qi T, Wang H, Tang H, Zhang J, Xing C (2014) Development of a candidate gene marker for Rf1 based on a PPR gene in cytoplasmic male sterile CMS-D2 Upland cotton. Mol Breed 34:231–240

    Article  Google Scholar 

  • Wu Y, Min L, Wu Z, Yang L, Zhu L, Yang X, Yuan D, Guo X, Zhang X (2015) Defective pollen wall contributes to male sterility in the male sterile line 1355A of cotton. Sci Rep 5:9608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu J, Zhang M, Zhang B, Zhang X, Guo L, Qi T, Wang H, Zhang J, Xing C (2017) Genome-wide comparative transcriptome analysis of CMS-D2 and its maintainer and restorer lines in upland cotton. BMC Genomics 18:454

    Article  PubMed  PubMed Central  Google Scholar 

  • Yan J, Yao Y, Hong S, Yang Y, Shen C, Zhang Q, Zhang D, Zou T, Yin P (2019) Delineation of pentatricopeptide repeat codes for target RNA prediction. Nucleic Acids Res 47:3728–3738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang L, Wu Y, Zhang M, Zhang J, Stewart JM, Xing C, Wu J, Jin S (2018) Transcriptome, cytological and biochemical analysis of cytoplasmic male sterility and maintainer line in CMS-D8 cotton. Plant Mol Biol 97:537–551

    Article  CAS  PubMed  Google Scholar 

  • Yin J, Guo W, Yang L, Liu L, Zhang T (2006) Physical mapping of the Rf1 fertility-restoring gene to a 100 kb region in cotton. Theor Appl Genet 112:1318–1325

    Article  CAS  PubMed  Google Scholar 

  • Yu C, Wang L, Xu S, Zeng Y, He C, Chen C, Huang W, Zhu Y, Hu J (2015) Mitochondrial ORFH79 is essential for drought and salt tolerance in rice. Plant Cell Physiol 56:2248–2258

    CAS  PubMed  Google Scholar 

  • Zhang JF, Stewart JM (2001) Inheritance and genetic relationships of the D8 and D2–2 restorer genes for cotton cytoplasmic male sterility. Crop Sci 41:289–294

    Article  Google Scholar 

  • Zhang J, Stewart JM (2004) Identification of molecular markers linked to the fertility restorer genes for CMS-D8 in cotton. Crop Sci 44:1209–1217

    Article  CAS  Google Scholar 

  • Zhang B, Zhang X, Guo L, Qi T, Wang H, Tang H, Qiao X, Shahzad K, Xing C, Wu J (2018) Genome-wide analysis of Rf-PPR-like (RFL) genes and a new InDel marker development for Rf1 gene in cytoplasmic male sterile CMS-D2 Upland cotton. J Cotton Res 1:12

    Article  Google Scholar 

  • Zhao C, Zhao G, Geng Z, Wang Z, Wang K, Liu S, Zhang H, Guo B, Geng J (2018) Physical mapping and candidate gene prediction of fertility restorer gene of cytoplasmic male sterility in cotton. BMC Genom 19:6

    Article  Google Scholar 

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Funding

This work was supported by the National Key Research and Development Plan of China (no. 2018YFD0100405).

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Authors and Affiliations

  1. National Key Laboratory of Crop Genetic Improvement, College of Plant Sciences and Technology, Huazhong Agricultural University, Wuhan, Hubei, China

    Bin Gao, Xianlong Zhang & Zhongxu Lin

  2. Yueyang Institute of Agricultural Science, Yueyang, 414000, Hunan, China

    Gaofeng Ren & Haiping Li

  3. Key Laboratory of Crop Physiology, Ecology and Genetic Breeding, College of Agronomy, Ministry of Education, Jiangxi Agricultural University, Nanchang, 330045, China

    Tianwang Wen

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  1. Bin Gao
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  2. Gaofeng Ren
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  5. Xianlong Zhang
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  6. Zhongxu Lin
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Contributions

ZXL conceived and designed the project. GFR and HPL planted and managed the mapping population. BG and GFR collected leaf samples and conducted phenotype investigation. We thank the high-performance computing center at National Key Laboratory of Crop Genetic Improvement in Huazhong Agricultural University. BG designed the analyzing pipeline. BG and TWW analyzed the sequencing data. BG performed the experiments. BG wrote the manuscript draft, XLZ and ZXL revised the manuscript.

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Correspondence to Zhongxu Lin.

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Gao, B., Ren, G., Wen, T. et al. A super PPR cluster for restoring fertility revealed by genetic mapping, homocap-seq and de novo assembly in cotton. Theor Appl Genet 135, 637–652 (2022). https://doi.org/10.1007/s00122-021-03990-0

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