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Pectin methylesterase inhibitor (PMEI) family can be related to male sterility in Chinese cabbage (Brassica rapa ssp. pekinensis)

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Abstract

Pectin-related genes play significant roles in pollen development and pollen tube growth, and their allelic variations are one of the major reasons for the abnormal development of male gametophyte. Currently, little is known about the role of the PMEI family in male sterility of plants. In this study, 97 putative PMEI genes were identified in Brassica rapa genome. By a phylogenetic analysis, the PMEI family was divided into 10 clades with highly conserved structural characteristics. The publically available RNA-seq data on different tissues of B. rapa accession Chiifu-401-42 revealed that 23 PMEI isoforms were flower-specific genes. We created a recessive genic male sterile mutant (ftms) in Chinese cabbage. This mutant was a doubled haploid line with stable inheritance, derived from Chinese cabbage ‘FT’ generated through a combination of radiation mutagenesis and isolated microspore culture. The transcriptome profiles of the floral buds of ftms and its wild-type line ‘FT’ were determined using RNA-seq. A total of 17 PMEI genes were found to be differentially expressed; all of them were down-regulated in ftms compared to their levels in ‘FT’. Consistent with the transcriptome data, all these genes were observed to be highly expressed in the floral buds of ‘FT’ using qRT–PCR analysis. Of these, eight genes were specifically expressed in the floral buds of ‘FT’; three of these (Bra019903, Bra014099, and Bra032239) were stamen-specific genes. The results contribute to further elucidation of the regulatory mechanisms underlying male sterility in Chinese cabbage.

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References

  • Abrouk M, Murat F, Pont C, Messing J, Jackson S, Faraut T, Tannier E, Plomion C, Cooke R, Feuillet C, Salse J (2010) Palaeogenomics of plants: synteny-based modelling of extinct ancestors. Trends Plant Sci 15:479–487

    Article  CAS  PubMed  Google Scholar 

  • An SH, Sohn KH, Choi HW, Hwang IS, Lee SC, Hwang BK (2008) Pepper pectin methyleasterase inhibitor protein CaPMEI1 is required for antifungal activity, basal disease resistance and abiotic stress tolerance. Planta 228:61–78

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Atmodjo MA, Sakuragi Y, Zhu X, Burrell AJ, Mohanty SS, Atwood JA, Orlando R, Scheller HV, Mohnen D (2011) Galacturonosyltransferase (GAUT)1 and GAUT7 are the core of a plant cell wall pectin biosynthetic homogalacturonan: galacturonosyltransferase complex. Proc Natl Acad Sci 108:20225–20230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren JY, Li WW, Nole WS (2009) MEME Suite: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths-Jones S, Khanna A, Marshall M, Moxon S, Sonnhammer EL (2004) The Pfam protein families database. Nucleic Acids Res 32:D138–D141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188

    Article  Google Scholar 

  • Birchler JA, Veitia RA (2007) The gene balance hypothesis: from classical genetics to modern genomics. Plant Cell 19:395–402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonavita A, Carratore V, Ciardiello MA, Giovane A, Servillo L, D’Avino R (2016) influence of pH on the structure and function of Kiwi pectin methylesterase inhibitor. J Agric Food Chem 64:5866–5876

    Article  CAS  PubMed  Google Scholar 

  • Camardella L, Carratore V, Ciardiello MA, Servillo L, Balestrieri C, Giovane A (2000) Kiwi prorein inhibitor of pectin methylestrtase: amino-acid sequence and structural importance of two disulfide bridges. Eur J Biochem 267:4561–4565

    Article  CAS  PubMed  Google Scholar 

  • Chebli Y, Geitmann A (2007) Mechanical principles governing pollen tube growth. Funct Plant Sci Biotechnol 1:232–245

    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 

  • Cheng F, Wu J, Fang L, Wang X (2012) Syntenic gene analysis between Brassica rapa and other Brassicaceae species. Front Plant Sci 3:198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng F, Mandáková T, Wu J, Xie Q, Lysak MA, Wang X (2013) Deciphering the diploid ancestral genome of the mesohexaploid Brassica rapa. Plant Cell 25:1541–1554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Di Matteo A, Giovane A, Raiola A, Camardella L, Bonivento D, De Lorenzo G, Cervone F, Bellincampi D, Tsernoglou D (2005) Structural basis for the interaction between pectin methylesterase and a specific inhibitor protein. Plant Cell 17:849–858

    Article  PubMed  PubMed Central  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Falasca G, D’Angeli S, Biasi R, Fattorini L, Matteucci M, Canini A, Altamura MM (2013) Tapetum and middle layer control male fertility in Actinidia deliciosa. Ann. Bot 112(6): 1045–1055

  • Fayant P, Girlanda O, Chebli Y, Aubin CE, Villemure I, Geitmann A (2010) Finite element model of polar growth in pollen tubes. Plant Cell 22:2579–2593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferguson C, Teeri TT, Siika-aho M, Read SM, Bacic A (1998) Location of cellulose and callose in pollen tubes and grains of Nicotiana tabacum. Planta 206:452–460

    Article  CAS  Google Scholar 

  • Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29–W37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Francis KE, Lam SY, Copenhaver GP (2006) Separation of Arabidopsis pollen tetrads is regulated by QUARTET1, a pectin methylesterase gene. Plant Physiol 142:1004–1013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Freeling M (2009) Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol 60:433–453

    Article  CAS  PubMed  Google Scholar 

  • Ganko EW, Meyers BC, Vision TJ (2007) Divergence in expression between duplicated genes in Arabidopsis. Mol Biol Evol 24:2298–2309

    Article  CAS  PubMed  Google Scholar 

  • Geitmann A (2010) How to shape a cylinder: pollen tube as a model system for the generation of complex cellular geometry. Sex Plant Reprod 23:63–71

    Article  PubMed  Google Scholar 

  • Hafidh S, Fila J, Honys D (2016) Male gametophyte development and function in angiosperms: a general concept. Plant Reprod 29:31–51

    Article  PubMed  Google Scholar 

  • Harholt J, Suttangkakul A, Vibe Scheller H (2010) Biosynthesis of pectin. Plant Physiol 153:384–395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Havey MJ (2004) The use of cytoplasmic male sterility for hybrid seed production. Mol Biol Biotechnol Plant Organelles 623–634

  • Hong CP, Kwon SJ, Kin JS, Yang TJ, Park BS, Lim YP (2008) Progress in understanding and sequencing the genome of Brassica rapa. Int J Plant Genomics 2008:582837

  • Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297

    Article  PubMed  Google Scholar 

  • Huang SN, Liu ZY, Li DY, Yao RP, Meng Q, Feng H (2014) Screening of Chinese cabbage mutant produced by 60Co-ray mutagenesis of isolated microspore cultures. Plant Breeding 133:480–488

    Article  CAS  Google Scholar 

  • Huang Z, Duan W, Song X, Tang J, Wu P, Zhang B, Hou X (2015) Retention, Molecular Evolution, and Expression Divergence of the Auxin/Indole Acetic Acid and Auxin Response Factor Gene Families in Brassica Rapa Shed Light on Their Evolution Patterns in Plants. Genome Biol Evol 8:302–316

    Article  PubMed  PubMed Central  Google Scholar 

  • Jiang L, Yang SL, Xie LF, Puah CS, Zhang XQ, Yang WC, Sundaresan V, Ye D (2005) VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell 17:584–596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:D480–D484

    Article  CAS  PubMed  Google Scholar 

  • Koch MA, Haubold B, Mitchell-Olds T (2000) Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol Biol Evol 17:1483–1498

    Article  CAS  PubMed  Google Scholar 

  • Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R. Horsman D, Jone SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) Molecular evolutionary genetics analysis version 7.0 for bigger database. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  Google Scholar 

  • Lee TH, Tang H, Wang X, Paterson AH (2013) PGDD: a database of gene and genome duplication in plants. Nucleic Acids Res 41:D1152–D1158

    Article  CAS  PubMed  Google Scholar 

  • Lei R, Li X, Ma Z, Lv Y, Hu Y, Yu D (2017) Arabidopsis WRKY2 and WRKY34 transcription factors interact with VQ20 protein to modulate pollen development and function. Plant J. https://doi.org/10.1111/tpj.13619

    PubMed  Google Scholar 

  • Leroux C, Bouton S, Kiefer-Meyer MC, Fabrice TN, Mareck A, Guénin S, Fournet F, Ringli C, Pelloux J, Driouich A, Lerouge P, Lehner A, Mollet JC (2015) Pectin methylesterase48 is invovled in Arabidopsis pollen grain germination. Plant Physiol Feb 167:367–380

    Article  CAS  Google Scholar 

  • Li HM, Rotter D, Bonos SA, Meyer WA, Belanger FC (2005a) Identification of a gene in the process of being lost from the genus Agrostis. Plant Physiol 138:2386–2395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J (2009) SOAP2: An improved ultrafast tool for short read alignment. Bio informatics 25:1966–1967

    CAS  Google Scholar 

  • Li H, Pinot F, Sauveplane V, Werck-Reichhart D, Diehl P, Schreiber L, Franke R, Zhang P, Chen L, Gao Y, Liang W, Zhang D (2010) Cytochrome P450 family member CYP704B2 catalyzes the {omega}-hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. Plant Cell 22:173–190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lu PL, Chai MF, Yang JG, Ning G, Wang GL, Ma H (2014) The Arabidopsis CALLOSE DEFECTIVE MICROSPORE1 gene is required for male fertility through regulating callose metabolism during microsporogenesis. Plant Physiol 164:1893–1904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miao YS, Li HY, Shen JB, Wang JQ, Jiang LW (2011) QUASIMODO 3 (QUA3) is a putative homogalacturonan methyltransferase regulating cell wall biosynthesis in Arabidopsis suspension-cultured cells. J Exp Bot 62:5063–5078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morris VJ, Gromer A, Kirby AR (2009) Architecture of intracellular networks in plant matrices. Struct Chem 20:255–261

    Article  CAS  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-SEq. Nat Methods 5:621–628

    Article  CAS  PubMed  Google Scholar 

  • Müller K, Levesque-Tremblay G, Fernandes A, Wormit A, Bartels S, Usadel B, Kermode A (2013) Overexpression of a pectin methylesterase inhibitor in Arabidopsis thaliana leads to altered growth morphology of the stem and defective organ separation. Plant Signal Behav 8:e26464

    Article  PubMed  PubMed Central  Google Scholar 

  • Palin RJ (2011) A comparison of cell wall properties of Arabidopsis thaliana. Dissertation, University of Birmingham

  • Raiola A, Camardella L, Giovane A, Mattei B, De Lorenzo G, Cervone F, Bellincampi D (2004) Two Arabidopsis thaliana genes encode functional pectin methylesterase inhibitors. FEBS Lett 557:199–203

    Article  CAS  PubMed  Google Scholar 

  • Rautengarten C, Usadel B, Neumetzler L, Hartmann J, Bussis D, Altmann T (2008) A subtilisin-like serine protease essential for mucilage release from Arabidopsis seed coats. Plant J 54:466–480

    Article  CAS  PubMed  Google Scholar 

  • Reca IB, Lionetti V, Camardella L, D’Avino R, Giardina T, Cervone F, Bellincampi D (2012) A functional pectin methylesterase inhibitor protein (SolyPMEI) is expressed during tomato fruit ripening and interacts with PME-1. Plant Mol Biol 79:429–442

    Article  CAS  PubMed  Google Scholar 

  • Schranz ME, Lysak MA, Mitchell-Olds T (2006) The ABC’ s of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci 11:535–542

    Article  CAS  PubMed  Google Scholar 

  • Sénéchal F, Wattier C, Rustérucci C, Pelloux J (2014) Homogalacturonan-modifying enzymes: structure, expression, and roles in plants. J Exp Bot 65:5125–5160

    Article  PubMed  PubMed Central  Google Scholar 

  • Sénéchal F, L’Enfant M, Domon JM, Rosiau E, Crépeau MJ, Surcouf O, Esquivel-Rodriguez J, Marcelo P, Mareck A, Guérineau F, Kim HR, Mravec J, Bonnin E, Jamet E, Kihara D, Lerouge P, Ralet MC, Pelloux J, Rayon C (2015a) Tuning of pectin methylesterification: pectin methylesterase inhibitor 7 modulates the processive activity of co-expressed pectin methylesterase 3 in a pH-dependent manner. J Biol Chem 290:23320–23335

    Article  PubMed  PubMed Central  Google Scholar 

  • Shi J, Cui M, Yang L, Kim YJ, Zhang D (2015) Genetic and biochemical mechanisms of pollen wall development. Trends Plant Sci 20:741–753

    Article  CAS  PubMed  Google Scholar 

  • Singh M, Kumar M, Thilges K, Cho MJ, Cigan AM (2017) MS26/CYP704B is required for anther and pollen wall development in bread wheat (Triticumaestivum L.) and combining mutations in all three homeologs causes male sterility. PLoS One 12:e0177632

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith BG, Harris PJ (1999) The polysaccharide composition of poales cell walls: Poaceae cell walls are not unique. Biochem Syst Ecol 27:33–53

    Article  CAS  Google Scholar 

  • Steiner-Lange S, Unte US, Eckstein L, Yang C, Wilson ZA, Schmelzer E, Dekker K, Saedler H (2003) Disruption of Arabidopsis thaliana MYB26 results in male sterility due to non-dehiscent anthers. Plant J 34:519–528

    Article  CAS  PubMed  Google Scholar 

  • Tang H, Wang X, Bowers JE, Ming R, Alam M, Paterson AH (2008) Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps. Genome Res 18:1944–1954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tong C, Wang X, Yu J, Wu J, Li W, Huang J, Dong C, Hua W, Liu S (2013) Comprehensive analysis of RNA-seq data reveals the complexity of the transcriptome in Brassica rapa. BMC Genomics 14:689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vedel F, Pla M, Vitart V, Gutierres S, Chétrit P, De Paepe R (1994) Molecular basis of nuclear and cytoplasmic male sterility in higher plants. Plant Physiol Biochem 32:601–608

    CAS  Google Scholar 

  • Wakabayashi K, Hoson T, Huber DJ (2003) Methyl de-esterification as a major factor regulating the extent of pectin depolymerization during fruit ripening: a comparison of the action of avocado (Persea americana) and tomato (Lycopersicon esculentum) polygalacturonases. J Plant Physiol 160:667–673

    Article  CAS  PubMed  Google Scholar 

  • Wan L, Zha W, Cheng X, Liu C, Lv L, Liu C, Wang Z, Du B, Chen R, Zhu L, He G (2011) A rice β-1, 3-glucanase gene Osg1 is required for callose degradation in pollen development. Planta 233:309–323

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Wang X, Tang H, Tan X, Ficklin SP, Feltus FA, Paterson AH (2011a) Modes of gene duplication contribute differently to genetic novelty and redundancy, but show parallels across divergent angiosperms. PLOS ONE 6:e28150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Wang H, Wang J et al (2011b) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1039

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Tang D, Luo Q, Jin Y, Shen Y, Wang K, Cheng Z (2012a) BRK1, a Bub1-related kinase, is essential for generating proper tension between homologous kinetochores at metaphase I of rice meiosis. Plant Cell 24:4961–4973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H, Kissinger JC, Paterson AH (2012b) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:e49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang YP, Tan X, Paterson AH (2013a) Different patterns of gene structure divergence following gene duplication in Arabidopsis. BMC Genomics 14:652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang M, Yuan D, Gao W, Li Y, Tan J, Zhang X (2013b) A comparative genome analysis of PME and PMEI families reveals the evolution of pectin metabolism in plant cell walls. PLoS One 8:e72082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF (1999) Protein identification and analysis tools on the ExPASy server. Methods Mol Biol 112:531–552

    CAS  PubMed  Google Scholar 

  • Wolf S, Grsic-Rausch S, Rausch T, Greiner S (2003) Identification of pollen-expressed pectin methylesterase inhibitors in Arabidopsis. FEBS Lett 555:551–555

    Article  CAS  PubMed  Google Scholar 

  • Wolf S, Mouille G, Pelloux J (2009) Homogalacturonan methylesterification and plant development. Mol Plant 2:851–860

    Article  CAS  PubMed  Google Scholar 

  • Woriedh M, Wolf S, Márton ML, Hinze A, Gahrtz M, Becker D, Dresselhaus T (2013) External application of gametophyte-specific ZmPMEI1 induces pollen tube burst in maize. Plant Reprod 26:255–226

    Article  CAS  PubMed  Google Scholar 

  • Wu YL, Min L, Wu ZC, Yang L, Zhu LF, Yang XY, Yuan DJ, Guo XP, Zhang XL (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 

  • Yang ZL, Liu HJ, Wang XR, Zeng QY (2013) Molecular evolution and expression divergence of the Populus polygalacturonase supergene family shed light on the evolution of increasingly complex organs in plants. New Phytol 197:1353–1365

    Article  CAS  PubMed  Google Scholar 

  • Zhang GY, Feng J, Wu J, Wang XW (2010) BoPMEI1, pollen-specific pectin methyleasterase inhibitor, has an essential role in pollen tube growth. Planta 231:1323–1334

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Xiao J, Wu J, Zhang H, Liu G, Wang X, Dai L (2012) ParaAT: a parallel tool for constructing multiple protein-coding DNA alignments. Biochem Biophys Res Commun 419:779–781

    Article  CAS  PubMed  Google Scholar 

  • Zhou SR, Wang Y, Li W, Zhao Z, Ren Y, Wang Y, Gu S, Lin Q, Wang D, Jiang L, Su N, Zhang X, Liu L, Cheng Z, Lei C, Wang J, Guo X, Wu F, Ikehashi H, Wang H, Wan J (2011) Pollen semi-sterility1 encodes a kinesin-1-like protein important for male meiosis, anther dehiscence, and fertility in rice. Plant Cell 23:111–129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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  1. Liaoning Key Lab of Genetics and Breeding for Cruciferous Vegetable Crops, Department of Horticulture, Shenyang Agricultural University, Shenyang, 110866, People’s Republic of China

    Chong Tan, Zhiyong Liu, Shengnan Huang, Chengyu Li, Jie Ren, Xiaoyan Tang, Wenjie Liu, Shenling Peng & Hui Feng

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  1. Chong Tan
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This work was supported by grants from the National Natural Science Foundation of China (No. 31672144).

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Tan, C., Liu, Z., Huang, S. et al. Pectin methylesterase inhibitor (PMEI) family can be related to male sterility in Chinese cabbage (Brassica rapa ssp. pekinensis). Mol Genet Genomics 293, 343–357 (2018). https://doi.org/10.1007/s00438-017-1391-4

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