Male sterile 28 encodes an ARGONAUTE family protein essential for male fertility in maize

Springer Science and Business Media LLC - Tập 29 Số 2 - Trang 189-201 - 2021
Yunfei Li, Yuxin Huang, Lingling Pan, Yue Zhao, Wei Huang, Weiwei Jin

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An X, Dong Z, Tian Y, Xie K, Wu S, Zhu T, Zhang D, Zhou Y, Niu C, Ma B, Hou Q, Bao J, Zhang S, Li Z, Wang Y, Yan T, Sun X, Zhang Y, Li J, Wan X (2019) ZmMs30 encoding a novel GDSL lipase is essential for male fertility and valuable for hybrid breeding in maize. Mol Plant 12:343–359

Anders S, Pyl PT, Huber W (2015) HTSeq-a python framework to work with high-throughput sequencing data. Bioinformatics 31:166–169

Belanger S, Pokhrel S, Czymmek KJ, Meyers BC (2020) Pre-meiotic, 24-nt reproductive phasiRNAs are abundant in anthers of wheat and barley but not rice and maize. Plant Physiol 2020:00816

Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, Benning C (1998) AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J 17:170–180

Carmell MA, Girard A, van de Kant HJ, Bourc’his D, Bestor TH, de Rooij DG, Hannon GJ (2007) MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell 12:503–514

Chen X, Zhang H, Sun H, Luo H, Zhao L, Dong Z, Yan S, Zhao C, Liu R, Xu C, Li S, Chen H, Jin W (2017) IRREGULAR POLLEN EXINE1 is a novel factor in anther cuticle and pollen exine formation. Plant Physiol 173:307–325

Cigan AM, Unger E, Xu R, Kendall T, Fox TW (2001) Phenotypic complementation of ms45 maize requires tapetal expression of MS45. Sex Plant Reprod 14:135–142

Das S, Swetha C, Pachamuthu K, Nair A, Shivaprasad PV (2020) Loss of function of Oryza sativa Argonaute 18 induces male sterility and reduction in phased small RNAs. Plant Reprod 33:59–73

Ding L, Yan SS, Jiang L, Zhao WS, Ning K, Zhao JY, Liu XF, Zhang J, Wang Q, Zhang XL (2015) HANABA TARANU (HAN) Bridges meristem and organ primordia boundaries through PINHEAD, JAGGED, BLADE-ON-PETIOLE2 and CYTOKININ OXIDASE 3 during flower development in Arabidopsis. PLoS Genet 11:e1005479

Field S, Thompson B (2016) Analysis of the maize dicer-like1 mutant, fuzzy tassel, implicates microRNAs in anther maturation and dehiscence. PLoS One 11:e0146534

Goldberg RB (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11:297–322

Golubovskaya IN, Sitnikova DV (1980) Three meiotic mutations of maize, causing irregular segregation of chromosomes in the first division of meiosis. Genetika 16:656–666

Hutvagner G, Simard MJ (2008) Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol 9:22–32

Kelliher T, Walbot V (2011) Emergence and patterning of the five cell types of the Zea mays anther locule. Dev Biol 350:32–49

Komiya R, Ohyanagi H, Niihama M, Watanabe T, Nakano M, Kurata N, Nonomura K (2014) Rice germline-specific Argonaute MEL1 protein binds to phasiRNAs generated from more than 700 lincRNAs. Plant J 78:385–397

Lei X, Liu B (2019) Tapetum-dependent male meiosis progression in plants: increasing evidence emerges. Front Plant Sci 10:1667

Lin HF, Spradling AC (1997) A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development 124:2463–2476

Liu H, Nonomura KI (2016) A wide reprogramming of histone H3 modifications during male meiosis I in rice is dependent on the Argonaute protein MEL1. J Cell Sci 129:3553–3561

Liu C, Shen Y, Qin B, Wen H, Cheng J, Mao F, Shi W, Tang D, Du G, Li Y, Wu Y, Cheng Z (2020) Oryza sativa RNA-dependent RNA polymerase 6 contributes to double-strand break formation in meiosis. Plant Cell 32(10):3273–3289

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

Lu XD, Liu JS, Ren W, Yang Q, Chai ZG, Chen RM, Wang L, Zhao J, Lang ZH, Wang HY, Fan YL, Zhao JR, Zhang CY (2018) Gene-indexed mutations in maize. Mol Plant 11:496–504

Ma Z, Zhang X (2018) Actions of plant Argonautes: predictable or unpredictable? Curr Opin Plant Biol 45:59–67

Mallory A, Vaucheret H (2010) Form, function, and regulation of ARGONAUTE proteins. Plant Cell 22:3879–3889

Moon J, Skibbe D, Timofejeva L, Wang CJ, Kelliher T, Kremling K, Walbot V, Cande WZ (2013) Regulation of cell divisions and differentiation by MALE STERILITY32 is required for anther development in maize. Plant J 76:592–602

Nan GL, Zhai J, Arikit S, Morrow D, Fernandes J, Mai L, Nguyen N, Meyers BC, Walbot V (2017) MS23, a master basic helix-loop-helix factor, regulates the specification and development of the tapetum in maize. Development 144:163–172

Nelms B, Walbot V (2019) Defining the developmental program leading to meiosis in maize. Science 364:52–56

Nishimura A, Ito M, Kamiya N, Sato Y, Matsuoka M (2002) OsPNH1 regulates leaf development and maintenance of the shoot apical meristem in rice. Plant J 30:189–201

Nonomura K, Morohoshi A, Nakano M, Eiguchi M, Miyao A, Hirochika H, Kurata N (2007) A germ cell specific gene of the ARGONAUTE family is essential for the progression of premeiotic mitosis and meiosis during sporogenesis in rice. Plant Cell 19:2583–2594

Olmedo-Monfil V, Durán-Figueroa N, Arteaga-Vázquez M, Demesa-Arévalo E, Autran D, Grimanelli D, Slotkin RK, Martienssen RA, Vielle-Calzada J-P (2010) Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464:628–632

Piffanelli P, Ross JHE, Murphy DJ (1998) Biogenesis and function of the lipidic structures of pollen grains. Sex Plant Reprod 11:65–80

Qian Y, Cheng Y, Cheng X, Jiang H, Zhu S, Cheng B (2011) Identification and characterization of Dicer-like, Argonaute and RNA-dependent RNA polymerase gene families in maize. Plant Cell Rep 30:1347–1363

Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140

Saito K, Nishida KM, Mori T, Kawamura Y, Miyoshi K, Nagami T, Siomi H, Siomi MC (2006) Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes Dev 20:2214–2222

Scott RJ, Spielman M, Dickinson HG (2004) Stamen structure and function. Plant Cell 16(Suppl):S46–S60

Singh M, Goel S, Meeley RB, Dantec C, Parrinello H, Michaud C, Leblanc O, Grimanelli D (2011) Production of viable gametes without meiosis in maize deficient for an ARGONAUTE protein. Plant Cell 23:443–458

Singh RK, Gase K, Baldwin IT, Pandey SP (2015) Molecular evolution and diversification of the Argonaute family of proteins in plants. BMC Plant Biol 15:23

Skibbe DS, Schnable PS (2005) Male sterility in maize. Maydica 50:367–376

Somaratne Y, Tian Y, Zhang H, Wang M, Huo Y, Cao F, Zhao L, Chen H (2017) ABNORMAL POLLEN VACUOLATION1 (APV1) is required for male fertility by contributing to anther cuticle and pollen exine formation in maize. Plant J 90:96–110

Sun W, Xiang X, Zhai L, Zhang D, Cao Z, Liu L, Zhang Z (2018) AGO18b negatively regulates determinacy of spikelet meristems on the tassel central spike in maize. J Integr Plant Biol 60:65–78

Tan H, Liang W, Hu J, Zhang D (2012) MTR1 encodes a secretory fasciclin glycoprotein required for male reproductive development in rice. Dev Cell 22:1127–1137

Teng C, Zhang H, Hammond R, Huang K, Meyers BC, Walbot V (2020) Dicer-like 5 deficiency confers temperature-sensitive male sterility in maize. Nat Commun 11:2912

Timofejeva L, Skibbe DS, Lee S, Golubovskaya I, Wang R, Harper L, Walbot V, Cande WZ (2013) Cytological characterization and allelism testing of anther developmental mutants identified in a screen of maize male sterile lines. G3 (Bethesda) 3:231–249

Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105–1111

Tsou CH, Cheng PC, Tseng CM, Yen HJ, Fu YL, You TR, Walden DB (2015) Anther development of maize (Zea mays) and longstamen rice (Oryza longistaminata) revealed by cryo-SEM, with foci on locular dehydration and pollen arrangement. Plant Reprod 28:47–60

Tucker MR, Okada T, Hu Y, Scholefield A, Taylor JM, Koltunow AM (2012) Somatic small RNA pathways promote the mitotic events of megagametogenesis during female reproductive development in Arabidopsis. Development 139:1399–1404

Vaucheret H (2008) Plant ARGONAUTES. Trends Plant Sci 13:350–358

Wan X, Wu S, Li Z, Dong Z, An X, Ma B, Tian Y, Li J (2019) Maize genic male-sterility genes and their applications in hybrid breeding: progress and perspectives. Mol Plant 12:321–342

Wan X, Wu S, Li Z, An X, Tian Y (2020) Lipid metabolism: critical roles in male fertility and other aspects of reproductive development in plants. Mol Plant 13:955–983

Wang CJ, Nan GL, Kelliher T, Timofejeva L, Vernoud V, Golubovskaya IN, Harper L, Egger R, Walbot V, Cande WZ (2012) Maize multiple archesporial cells 1 (mac1), an ortholog of rice TDL1A, modulates cell proliferation and identity in early anther development. Development 139:2594–2603

Williams ME (1995) Genetic engineering for pollination control. Trends Biotechnol 13:344–349

Yang WC, Sundaresan V (2000) Genetics of gametophyte biogenesis in Arabidopsis. Curr Opin Plant Biol 3:53–57

Yang SL, Xie LF, Mao HZ, Puah CS, Yang WC, Jiang L, Sundaresan V, Ye D (2003) Tapetum determinant1 is required for cell specialization in the Arabidopsis anther. Plant Cell 15:2792–2804

Yi J, Moon S, Lee YS, Zhu L, Liang W, Zhang D, Jung KH, An G (2016) Defective tapetum cell death 1 (DTC1) regulates ROS levels by binding to metallothionein during tapetum degeneration. Plant Physiol 170:1611–1623

Yigit E, Batista PJ, Bei Y, Pang KM, Chen CC, Tolia NH, Joshua-Tor L, Mitani S, Simard MJ, Mello CC (2006) Analysis of the C. elegans Argonaute family reveals that distinct Argonautes act sequentially during RNAi. Cell 127:747–757

Zhai L, Sun W, Zhang K, Jia H, Liu L, Liu Z, Teng F, Zhang Z (2014) Identification and characterization of Argonaute gene family and meiosis-enriched Argonaute during sporogenesis in maize. J Integr Plant Biol 56:1042–1052

Zhai J, Zhang H, Arikit S, Huang K, Nan GL, Walbot V, Meyers BC (2015) Spatiotemporally dynamic, cell-type-dependent premeiotic and meiotic phasiRNAs in maize anthers. Proc Natl Acad Sci U S A 112:3146–3151

Zhang D, Yang L (2014) Specification of tapetum and microsporocyte cells within the anther. Curr Opin Plant Biol 17:49–55

Zhang H, Xia R, Meyers BC, Walbot V (2015) Evolution, functions, and mysteries of plant ARGONAUTE proteins. Curr Opin Plant Biol 27:84–90

Zhang L, Luo H, Zhao Y, Chen X, Huang Y, Yan S, Li S, Liu M, Huang W, Zhang X, Jin W (2018a) Maize male sterile 33 encodes a putative glycerol-3-phosphate acyltransferase that mediates anther cuticle formation and microspore development. BMC Plant Biol 18:318

Zhang D, Wu S, An X, Xie K, Dong Z, Zhou Y, Xu L, Fang W, Liu S, Liu S, Zhu T, Li J, Rao L, Zhao J, Wan X (2018b) Construction of a multicontrol sterility system for a maize male-sterile line and hybrid seed production based on the ZmMs7 gene encoding a PHD-finger transcription factor. Plant Biotechnol J 16:459–471

Zhang YC, Lei MQ, Zhou YF, Yang YW, Lian JP, Yu Y, Feng YZ, Zhou KR, He RR, He H, Zhang Z, Yang JH, Chen YQ (2020) Reproductive phasiRNAs regulate reprogramming of gene expression and meiotic progression in rice. Nat Commun 11:6031

Zheng S, Li J, Ma L, Wang H, Zhou H, Ni E, Jiang D, Liu Z, Zhuang C (2019) OsAGO2 controls ROS production and the initiation of tapetal PCD by epigenetically regulating OsHXK1 expression in rice anthers. Proc Natl Acad Sci U S A 116:7549–7558