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Comparative analysis of the transcriptome, methylome, and metabolome during pollen abortion of a seedless citrus mutant

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Abstract

Key Message

Pollen abortion could be mainly attributed to abnormal meiosis in the mutant. Multiomics analysis uncovered significant epigenetic variations between the mutant and its wild type during the pollen abortion process.

Abstract

Male sterility caused by aborted pollen can result in seedless fruit. A seedless Ponkan mandarin mutant (bud sport) was used to compare the transcriptome, methylome, and metabolome with its progenitor to understand the mechanism of citrus pollen abortion. Cytological observations showed that the anther of the mutant could form microspore mother cells, although the microspores failed to develop fertile pollen at the anther dehiscence stage. Based on pollen phenotypic analysis, pollen abortion could be mainly attributed to abnormal meiosis in the mutant. A transcriptome analysis uncovered the molecular mechanisms underlying pollen abortion between the mutant and its wild type. A total of 5421 differentially expressed genes were identified, and some of these genes were involved in the meiosis, hormone biosynthesis and signaling, carbohydrate, and flavonoid pathways. A total of 50,845 differentially methylated regions corresponding to 15,426 differentially methylated genes in the genic region were found between the mutant and its wild type by the methylome analysis. The expression level of these genes was negatively correlated with their methylation level, especially in the promoter regions. In addition, 197 differential metabolites were identified between the mutant and its wild type based on the metabolome analysis. The transcription and metabolome analysis further indicated that the expression of genes in the flavonoid, carbohydrate, and hormone metabolic pathways was significantly modulated in the pollen of the mutant. These results indicated that demethylation may alleviate the silencing of carbohydrate genes in the mutant, resulting in excessive starch and sugar hydrolysis and thereby causing pollen abortion in the mutant.

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Abbreviations

DAPI:

4′,6-Diamidino-2-phenylindole

DMRs:

Differentially methylated regions

DMGs:

Differentially methylated genes

FDR:

False discovery rate

GO:

Gene ontology

PCD:

Programmed cell death

ROS:

Reactive oxygen species

SEM:

Scanning electron microscopy

TEM:

Transmission electron microscope

WGBS:

Whole-genome bisulfite sequencing

References

  • Alexander MP (1969) Differential staining of aborted and nonaborted pollen. Stain Technol 44(3):117–122

    Article  CAS  PubMed  Google Scholar 

  • Bai S, Tuan PA, Saito T, Honda C, Hatsuyama Y, Ito A, Moriguchi T (2016) Epigenetic regulation of MdMYB1 is associated with paper bagging-induced red pigmentation of apples. Planta 244(3):573–586

    Article  CAS  PubMed  Google Scholar 

  • Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16(1):6–21

    Article  CAS  PubMed  Google Scholar 

  • Blankenberg D, Gordon A, Von Kuster G, Coraor N, Taylor J, Nekrutenko A (2010) Manipulation of FASTQ data with Galaxy. Bioinformatics 26(14):1783–1785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L, Liu YG (2014) Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65(1):579–606

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Gong L, Guo Z, Wang W, Zhang H, Liu X, Yu S, Xiong L, Luo J (2013) A novel integrated method for large-scale detection, identification, and quantification of widely targeted metabolites: application in the study of rice metabolomics. Mol Plant 6(6):1769–1780

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Guan X, Qin L, Zou T, Zhang Y, Wang J, Wang Y, Pan C, Lu G (2016) Downregulation of the mitogen-activated protein kinase SlMAPK7 gene results in pollen abortion in tomato. Plant Cell, Tissue Organ Cult 126(1):79–92

    Article  CAS  Google Scholar 

  • Cheng YJ, Guo WW, Yi HL, Pang XM, Deng X (2003) An efficient protocol for genomic DNA extraction from Citrus species. Plant Mol Biol Rep 21(2):177–178

    Article  Google Scholar 

  • Dao TTH, Linthorst HJM, Verpoorte R (2011) Chalcone synthase and its functions in plant resistance. Phytochem Rev 10(3):397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Hoon MJ, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20(9):1453–1454

    Article  PubMed  CAS  Google Scholar 

  • Fang YN, Qiu WM, Wang Y, Wu XM, Xu Q, Guo WW (2014) Identification of differentially expressed microRNAs from a male sterile Ponkan mandarin (Citrus reticulata Blanco) and its fertile wild type by small RNA and degradome sequencing. Tree Genet Genomes 10(6):1567–1581

    Article  Google Scholar 

  • Feucht W, Treutter D, Dithmar H, Polster J (2005) Flavanols in somatic cell division and male meiosis of tea (Camellia sinensis) anthers. Plant Biol 7(02):168–175

    Article  CAS  PubMed  Google Scholar 

  • Feucht W, Treutter D, Dithmar H, Polster J (2008) Microspore development of three coniferous species: affinity of nuclei for flavonoids. Tree Physiol 28(12):1783–1791

    Article  PubMed  Google Scholar 

  • Finnegan EJ, Kovac KA (2000) Plant DNA methyltransferases. In: Matzke MA, Matzke AJM (eds) Plant Gene Silencing. Springer, Dordrecht, pp 69–81

    Chapter  Google Scholar 

  • Foster TM, Aranzana MJ (2018) Attention sports fans! The far-reaching contributions of bud sport mutants to horticulture and plant biology. Horticult Res 5(1):44

    Article  CAS  Google Scholar 

  • Frank G, Pressman E, Ophir R, Althan L, Shaked R, Freedman M, Shen S, Firon N (2009) Transcriptional profiling of maturing tomato (Solanum lycopersicum L.) microspores reveals the involvement of heat shock proteins, ROS scavengers, hormones, and sugars in the heat stress response. J Exp Bot 60(13):3891–3908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo JX, Liu YG (2012) Molecular control of male reproductive development and pollen fertility in rice. J Integr Plant Biol 54(12):967–978

    Article  CAS  PubMed  Google Scholar 

  • Hadwiger JA, Wittenberg C, Richardson HE, de Barros Lopes M, Reed S (1989) A family of cyclin homologs that control the G1 phase in yeast. Proc Natl Acad Sci 86(16):6255–6259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu ZY, Zhang M, Wen QG, Wei J, Yi HL, Deng XX, Xu XH (2007) Abnormal microspore development leads to pollen abortion in a seedless mutant of ‘Ougan’ mandarin (Citrus suavissima Hort. ex Tanaka). J Am Soc Horticult Sci Am Soc Horticult Sci 132(6):777–782

    Article  Google Scholar 

  • Huang J-H, Wen S-X, Zhang Y-F, Zhong Q-Z, Yang L, Chen L-S (2017) Abnormal megagametogenesis results in seedlessness of a polyembryonic ‘Meiguicheng’ orange (Citrus sinensis) mutant created with gamma-rays. Sci Horticult 217:73–83

    Article  Google Scholar 

  • Jewell JB, Browse J (2016) Epidermal jasmonate perception is sufficient for all aspects of jasmonate-mediated male fertility in Arabidopsis. Plant J 85(5):634–647

    Article  CAS  PubMed  Google Scholar 

  • Jürgen P, Heike D, Feucht W (2003) Are histones the targets for flavan-3-ols (catechins) in nuclei? Biol Chem 384(7):997–1006

    Google Scholar 

  • Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T (2007) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:D480–D484

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kerzendorfer C, Vignard J, Pedrosa-Harand A, Siwiec T, Akimcheva S, Jolivet S, Sablowski R, Armstrong S, Schweizer D, Mercier R, Schlögelhofer P (2006) The Arabidopsis thaliana MND1 homologue plays a key role in meiotic homologous pairing, synapsis and recombination. J Cell Sci 119(12):2486

    Article  CAS  PubMed  Google Scholar 

  • Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12(4):357–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koes R, Verweij W, Quattrocchio F (2005) Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci 10(5):236–242

    Article  CAS  PubMed  Google Scholar 

  • Kolas NK, Cohen PE (2004) Novel and diverse functions of the DNA mismatch repair family in mammalian meiosis and recombination. Cytogenet Genome Res 107(3–4):216–231

    Article  CAS  PubMed  Google Scholar 

  • Kolde R (2015) pheatmap: Pretty Heatmaps. R package version 1.0. 8

  • Kovaleva L, Voronkov A, Zakharova E, Andreev I (2018) ABA and IAA control microsporogenesis in Petunia hybrida L. Protoplasma 255(3):751–759

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Chen M, Wei W, Liang D, Li T (1999) Early-maturing seedless Shatian pumelo and pollen abortion. Acta Laser Biol Sin 3:51–53

    Google Scholar 

  • Li Y, Ding X, Wang X, He T, Zhang H, Yang L, Wang T, Chen L, Gai J, Yang S (2017) Genome-wide comparative analysis of DNA methylation between soybean cytoplasmic male-sterile line NJCMS5A and its maintainer NJCMS5B. BMC Genom 18(1):596

    Article  CAS  Google Scholar 

  • Lister R, O’Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, Ecker JR (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133(3):523–536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu L, Fan X (2013) Tapetum: regulation and role in sporopollenin biosynthesis in Arabidopsis. Plant Mol Biol 83(3):165–175

    Article  CAS  PubMed  Google Scholar 

  • Liu G, Xia Y, Liu T, Dai S, Hou X (2018) The DNA methylome and association of differentially methylated regions with differential gene expression during heat stress in Brassica rapa. Int J Mol Sci 19(5):1414

    Article  PubMed Central  CAS  Google Scholar 

  • Lorincz MC, Dickerson DR, Schmitt M, Groudine M (2004) Intragenic DNA methylation alters chromatin structure and elongation efficiency in mammalian cells. Nat Struct Mol Biol 11(11):1068–1075

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Min L, Wang M, Wang C, Zhao Y, Li Y, Fang Q, Wu Y, Xie S, Ding Y (2018) Disrupted genome methylation in response to high temperature has distinct affects on microspore abortion and anther indehiscence. Plant Cell 30(7):1387–1403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mao X, Cai T, Olyarchuk JG, Wei L (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21(19):3787–3793

    Article  CAS  PubMed  Google Scholar 

  • Min L, Li Y, Hu Q, Zhu L, Gao W, Wu Y, Ding Y, Liu S, Yang X, Zhang X (2014) Sugar and auxin signaling pathways respond to high-temperature stress during anther development as revealed by transcript profiling analysis in cotton. Plant Physiol 164(3):1293–1308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Napoli CA, Fahy D, Wang H-Y, 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(2):615–622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliver SN, Dennis ES, Dolferus R (2007) ABA regulates apoplastic sugar transport and is a potential signal for cold-induced pollen sterility in rice. Plant Cell Physiol 48(9):1319–1330

    Article  CAS  PubMed  Google Scholar 

  • Oshino T, Abiko M, Saito R, Ichiishi E, Endo M, Kawagishi-Kobayashi M, Higashitani A (2007) Premature progression of anther early developmental programs accompanied by comprehensive alterations in transcription during high-temperature injury in barley plants. Mol Genet Genom 278(1):31–42

    Article  CAS  Google Scholar 

  • Pan X, Welti R, Wang X (2010) Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. Nat Protoc 5(6):986–992

    Article  CAS  PubMed  Google Scholar 

  • Qian M, Sun Y, Allan AC, Teng Y, Zhang D (2014) The red sport of ‘Zaosu’ pear and its red-striped pigmentation pattern are associated with demethylation of the PyMYB10 promoter. Phytochemistry 107:16–23

    Article  CAS  PubMed  Google Scholar 

  • Qiu W-M, Zhu A-D, Wang Y, Chai L-J, Ge X-X, Deng X-X, Guo W-W (2012) Comparative transcript profiling of gene expression between seedless Ponkan mandarin and its seedy wild type during floral organ development by suppression subtractive hybridization and cDNA microarray. BMC Genom 13:397

    Article  CAS  Google Scholar 

  • Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57(1):675–709

    Article  CAS  PubMed  Google Scholar 

  • Rupali D, Chamusco KC, Chourey PS (2002) Starch biosynthesis during pollen maturation is associated with altered patterns of gene expression in maize. Plant Physiol 130(4):1645–1656

    Article  CAS  Google Scholar 

  • Sakata T, Oshino T, Miura S, Tomabechi M, Tsunaga Y, Higashitani N, Miyazawa Y, Takahashi H, Watanabe M, Higashitani A (2010) Auxins reverse plant male sterility caused by high temperatures. Proc Natl Acad Sci 107(19):8569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanchez-Moran E, Armstrong S (2014) Meiotic chromosome synapsis and recombination in Arabidopsis thaliana: new ways of integrating cytological and molecular approaches. Chromosome Res 22(2):179–190

    Article  CAS  PubMed  Google Scholar 

  • Schreiber DN, Bantin J, Dresselhaus T (2004) The MADS box transcription factor ZmMADS2 is required for anther and pollen maturation in maize and accumulates in apoptotic bodies during anther dehiscence. Plant Physiol 134(3):1069–1079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smallwood SA, Lee HJ, Angermueller C, Krueger F, Saadeh H, Peat J, Andrews SR, Stegle O, Reik W, Kelsey G (2014) Single-cell genome-wide bisulfite sequencing for assessing epigenetic heterogeneity. Nat Methods 11(8):817–820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song F, Smith JF, Kimura MT, Morrow AD, Matsuyama T, Nagase H, Held WA (2005) Association of tissue-specific differentially methylated regions (TDMs) with differential gene expression. Proc Natl Acad Sci 102(9):3336–3341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun D, Xi Y, Rodriguez B, Park HJ, Tong P, Meong M, Goodell MA, Li W (2014) MOABS: model based analysis of bisulfite sequencing data. Genome Biol 15(2):R38

    Article  PubMed  PubMed Central  Google Scholar 

  • Tang H, Song Y, Guo J, Wang J, Zhang L, Niu N, Ma S, Zhang G, Zhao HJPP (2018) Physiological and metabolome changes during anther development in wheat (Triticum aestivum L.). Plant Physiol Biochem 132:18–32

    Article  CAS  PubMed  Google Scholar 

  • Taylor LP, Grotewold E (2005) Flavonoids as developmental regulators. Curr Opin Plant Biol 8(3):317–323

    Article  CAS  PubMed  Google Scholar 

  • Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28(5):511–515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuchiya E, Uno M, Kiguchi A, Masuoka K, Kanemori Y, Okabe S, Mikayawa T (1992) The Saccharomyces cerevisiae NPS1 gene, a novel CDC gene which encodes a 160 kDa nuclear protein involved in G2 phase control. EMBO J 11(11):4017–4026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Varoquaux F, Blanvillain R, Delseny M, Gallois P (2000) Less is better: new approaches for seedless fruit production. Trends in Biotechnol 18(6):233–242

    Article  CAS  Google Scholar 

  • Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26(1):136–138

    Article  PubMed  CAS  Google Scholar 

  • Wang D, Cai J, Zhu B-Q, Wu G-F, Duan C-Q, Chen G, Shi Y (2015) Study of free and glycosidically bound volatile compounds in air-dried raisins from three seedless grape varieties using HS-SPME with GC-MS. Food Chem 177:346–353

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Hong T, Wan J, Chen W, Liu X, Luo J, Xu J, Zhang H (2016) Spatio-temporal distribution and natural variation of metabolites in citrus fruits. Food Chem 199:8–17

    Article  CAS  PubMed  Google Scholar 

  • Wilson ZA, Zhang D-B (2009) From Arabidopsis to rice: pathways in pollen development. J Exp Bot 60(5):1479–1492

    Article  CAS  PubMed  Google Scholar 

  • Wu GA, Prochnik S, Jenkins J, Salse J, Hellsten U, Murat F, Perrier X, Ruiz M, Scalabrin S, Terol J (2014) Sequencing of diverse mandarin, pummelo and orange genomes reveals complex history of admixture during citrus domestication. Nat Biotechnol 32(7):656–662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie CT, Yang YH, Qiu YL, Zhu XY, Tian HQ (2005) Cytochemical investigation of genic male-sterility in Chinese cabbage. Sex Plant Reprod 18(2):75–80

    Article  Google Scholar 

  • Xu J, Wang X, Cao H, Xu H, Xu Q, Deng X (2017) Dynamic changes in methylome and transcriptome patterns in response to methyltransferase inhibitor 5-azacytidine treatment in citrus. DNA Res 24(5):509–522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu J, Zhou S, Gong X, Song Y, van Nocker S, Ma F, Guan Q (2018) Single-base methylome analysis reveals dynamic epigenomic differences associated with water deficit in apple. Plant Biotechnol J 16(2):672–687

    Article  CAS  PubMed  Google Scholar 

  • Yang C, Vizcay-Barrena G, Conner K, Wilson ZA (2007) MALE STERILITY1 is required for tapetal development and pollen wall biosynthesis. Plant Cell 19(11):3530–3548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang YU, Wei W, Yang XL, Zeng ZF, Yue-Jin LI, Shan LI, Yun-Guo Z (2011) Causes of seedless forming of nanfeng tangerine. Acta Horticult Sin 4:631–636

    Google Scholar 

  • Yang J, Tian L, Sun M-X, Huang X-Y, Zhu J, Guan Y-F, Jia Q-S, Yang Z-N (2013) AUXIN RESPONSE FACTOR 17 is essential for pollen wall pattern formation in Arabidopsis. Plant Physiol 162(2):720–731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ye W, Qin Y, Ye Z, Silva JATD, Zhang L, Wu X, Lin S, Hu G (2009) Seedless mechanism of a new mandarin cultivar ‘Wuzishatangju’ (Citrus reticulata Blanco). Plant Sci 177(1):19–27

    Article  CAS  Google Scholar 

  • Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11(2):R14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang H, Liang W, Yang X, Luo X, Jiang N, Ma H, Zhang D (2010) Carbon starved anther encodes a MYB domain protein that regulates sugar partitioning required for rice pollen development. Plant Cell 22(3):672–689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang SW, Huang GX, Ding F, He XH (2012) Mechanism of seedlessness in a new lemon cultivar ‘Xiangshui’ [Citrus limon (L.) Burm. F.]. Sex Plant Reprod 25(4):337–345

    Article  PubMed  Google Scholar 

  • Zhang D, Liu D, Lv X, Wang Y, Xun Z, Liu Z, Li F, Lu H (2014) The cysteine protease CEP1, a key executor involved in tapetal programmed cell death, regulates pollen development in Arabidopsis. Plant Cell 26(7):2939–2961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Cao Q, Zhou P, Jia G (2017a) Meiotic chromosome behavior of the male-fertile allotriploid lily cultivar ‘Cocossa’. Plant Cell Rep 36(10):1–13

    Article  CAS  Google Scholar 

  • Zhang YL, Li FZ, Feng X, Yang H, Zhu AX, Pang J, Han L, Zhang TT, Yao XL, Wang F (2017b) Genome-wide analysis of DNA methylation profiles on sheep ovaries associated with prolificacy using whole-genome Bisulfite sequencing. BMC Genom 18(1):759

    Article  CAS  Google Scholar 

  • Zhu E, You C, Wang S, Cui J, Niu B, Wang Y, Qi J, Ma H, Chang F (2015) The DYT 1-interacting proteins bHLH010, bHLH089 and bHLH091 are redundantly required for Arabidopsis anther development and transcriptome. Plant J 83(6):976–990

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This research was supported financially by the National Major Research and Development Plan (2019YFD1000104), the National Natural Science Foundation of China (Grant Nos. 31772252, 31601743, and 31872045), and the Fundamental Research Funds for the Central Universities (2662018JC044).

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Authors and Affiliations

  1. Key Laboratory of Horticultural Plant Biology (Ministry of Education), College of Horticulture and Forestry Science, Huazhong Agricultural University, Wuhan, 430070, China

    Li-Xia Ye, Zhi-Meng Gan, Wen-Feng Wang, Zong-Zhou Xie, Chun-Gen Hu & Jin-Zhi Zhang

  2. Institute of Pomology and Tea, Hubei Academy of Agricultural Sciences, Wuhan, 430070, China

    Xiao-Yan Ai

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J.J.Z. and C.G.H. conceived the research plan and supervised the experiments. L.X.Y., Z.M.G., X.Y.A., Z.Z.X., and W.F.W. performed the experiments and analyzed the data. Z.J.Z. drafted the manuscript. All authors read and approved the final manuscript. All authors read and approved the final manuscript.

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Correspondence to Jin-Zhi Zhang.

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Ye, LX., Gan, ZM., Wang, WF. et al. Comparative analysis of the transcriptome, methylome, and metabolome during pollen abortion of a seedless citrus mutant. Plant Mol Biol 104, 151–171 (2020). https://doi.org/10.1007/s11103-020-01034-7

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