玉米籽粒形成的分子生物学基础

doi:10.3864/j.issn.0578-1752.2019.20.001

摘要/Abstract

摘要：

玉米单穗籽粒产量由穗粒数和粒重两因子组成。单个果穗上所着生的籽粒数与雌花序建成和小花分化密切相关,因此,控制花序形态建成和小花发育的基因可能直接或间接地参与穗粒数调控。玉米成熟籽粒主要由源于母本组织的种皮和经双受精产生的胚和胚乳组成,且胚和胚乳占成熟籽粒的绝大部分,直接影响粒重。文中主要从“CLAVATA（CLV）-WUSCHEL（WUS）负反馈调控途径、激素及其信号途径、花器官发育和小花性别决定”等方面总结了花序和小花发育相关基因及其与穗粒数的关系,描述了CLV-WUS途径中各基因在玉米雌花序上特异性表达的分生组织和基因间的调控关系,总结了生长素、赤霉素、细胞分裂素和独脚金内酯等植物激素的相互作用网络,以及已克隆的玉米花器官发育相关基因及其功能。从“线粒体基因转录本的加工和编辑、质体基因的转录和翻译及细胞核RNA转录与加工”3个方面总结了已克隆的影响胚和胚乳发育的相关基因,其中,大部分基因编码线粒体或质体定位的PPR蛋白。值得关注的是,近年来,研究发现了通过调节细胞核内RNA转录和加工而影响玉米籽粒发育的新途径。文章作者在基因水平上对玉米籽粒形成的分子生物学基础进行了简要总结,为进一步深入解析玉米产量形成的分子调控网络提供参考。同时,也就该研究领域今后可能的研究方向进行了讨论。

关键词: 玉米, 穗粒数, 粒重, 花序, 小花, 胚, 胚乳

Abstract:

Grain yield per ear of maize (Zea mays L.) is composed of both kernel number and grain weight. The number of kernels on an ear is determined by not only the number of kernel rows which is closely related to the inflorescence development, but also the number of fertile florets generated by the flower meristem. Therefore, those genes for inflorescence architecture and flower development are potentially involved in the genetic control of kernel number. Maize kernel is a single-seeded fruit comprised of the maternally derived pericarp, and embryo and endosperm derived from double fertilization. Both embryo and endosperm account for the vast majority of the mature kernel mass, and directly determine the kernel size and weight. In this paper, we outlined the genetic controls of kernel number with the emphasis on the inflorescence and floret related genes that are involved in the CLAVATA- WUSCHEL (CLV-WUS) feedback loop, hormone biosynthesis and signaling, floral organ development and sex determination. In particular, we described the regulatory network models for interplays among phytohormones including auxin, gibberellin, cytokinin and strigolactone in the inflorescence architecture and floral organ development. We also summarized those embryo and endosperm developmental genes involving in processing and editing of mitochondrial transcripts, transcription and translation of some chloroplast DNAs as well as nuclear RNAs. Most of these genes encode PPR proteins targeted to mitochondria or plastids. Recently, several studies have identified a new pathway to control kernel development by regulating the transcription and processing of pre-mRNA within the nucleus. Here, we also discussed the association between these genes and kernel number or kernel weight, and the potential areas of research for deciphering molecular mechanisms of grain yield in maize.

Key words: Zea mays L., kernel number per ear, kernel weight, inflorescence, floret, embryo, endosperm

赵然,蔡曼君,杜艳芳,张祖新. 玉米籽粒形成的分子生物学基础[J]. 中国农业科学, 2019, 52(20): 3495-3506.

Ran ZHAO,ManJun CAI,YanFang DU,ZuXin ZHANG. Molecular Basis of Kernel Development and Kernel Number in Maize (Zea mays L.)[J]. Scientia Agricultura Sinica, 2019, 52(20): 3495-3506.

0
/ / 推荐

导出引用管理器 EndNote|Reference Manager|ProCite|BibTeX|RefWorks

链接本文: https://www.chinaagrisci.com/CN/10.3864/j.issn.0578-1752.2019.20.001

https://www.chinaagrisci.com/CN/Y2019/V52/I20/3495

图/表 3

图1

图2

图3

参考文献 92

[1]	VOLLBRECHT E, SCHMIDT R J . Handbook of maize// BENNETZEN J L, HAKE S, eds. Development of the Inflorescences. New York: Springer, 2009: 13-40.
[2]	WILLIAMS L, FLETCHER J C . Stem cell regulation in the Arabidopsis shoot apical meristem. Current Opinion in Plant Biology, 2005,8:582-586.
[3]	SOMSSICH M, JE B I, SIMON R, JACKSON D . CLAVATA- WUSCHEL signaling in the shoot meristem. Development, 2016,143:3238-3248.
[4]	BOMMERT P, LUNDE C, NARDMANN J, VOLLBRECHT E, RUNNING M, JACKSON D, HAKE S, WERR W . thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine- rich repeat receptor-like kinase. Development, 2005,132(6):1235-1245.
[5]	BOMMERT P, NAGASAWA N S, JACKSON D . Quantitative variation in maize kernel row number is controlled by the FASCIATED EAR2 locus. Nature Genetics, 2013,45:334-337.
[6]	JE B I, GRUEL J, LEE K, BOMMERT P, AREVALO E D, EVELAND A L, WU Q, GOLDSHMIDT A, MEELEY R, BARTLETT M, KOMATSU M, SAKAI H, JÖNSSON H, JACKSON D . Signaling from maize organ primordia via FASCIATED EAR3 regulates stem cell proliferation and yield traits. Nature Genetics, 2016,48:785-791.
[7]	RODRIGUEZ-LEAL D, XU C, KWON C T, SOYARS C, DEMESA-AREVALO E, MAN J, LIU L, LEMMON Z H, JONES D S, VAN ECK J, JACKSON D P, BARTLETT M E, NIMCHUK Z L, LIPPMAN Z B . Evolution of buffering in a genetic circuit controlling plant stem cell proliferation. Nature Genetics, 2019,51(5):786-792.
[8]	BOMMERT P, JE B I, GOLDSHMIDT A, JACKSON D . The maize Gα gene COMPACT PLANT2 functions in CLAVATA signaling to control shoot meristem size. Nature, 2013,502:555-558.
[9]	JE BI, XU F, WU Q, LIU L, MEELEY R, GALLAGHER J P, CORCILIUS L, PAYNE R J, BARTLETT M E, JACKSON D . The CLAVATA receptor FASCIATED EAR2 responds to distinct CLE peptides by signaling through two downstream effectors. Elife, 2018,7:e35673.
[10]	CHUCK G S, BROWN J, MEELEY R, HAKE S . Maize SBP-box transcription factors unbranched2 and unbranched3 affect yield traits by regulating the rate of lateral primordia initiation. Proceedings of the National Academy of Sciences of the United States of America, 2014,111:18775-18780.
[11]	ZHANG D, SUN W, SINGH R, ZHENG Y, CAO Z, LI M, LUNDE C, HAKE S, ZHANG Z . GRF-interacting factor1 (gif1) regulates shoot architecture and meristem determinacy in maize. The Plant Cell, 2018,30:360-374.
[12]	DU Y, LIU L, LI M, FANG S, SHEN X, CHU J, ZHANG Z . UNBRANCHED3 regulates branching by modulating cytokinin biosynthesis and signaling in maize and rice. New Phytologist, 2016,214(2):721-733.
[13]	LIU L, DU Y, SHEN X, LI M, SUN W, HUANG J, LIU Z, TAO Y, ZHENG Y, YAN J, ZHANG Z . KRN4 controls quantitative variation in maize kernel row number. PLoS Genetics, 2015,11:e1005670.
[14]	PHILLIPS K A, SKIRPAN A L, LIU X, CHRISTENSEN A, SLEWINSKI T L, HUDSON C, BARAZESH S, COHEN J D, MALCOMBER S, MCSTEEN P . vanishing tassel2 encodes a grass-specific tryptophan aminotransferase required for vegetative and reproductive development in maize. The Plant Cell, 2011,23:550-566.
[15]	GALLAVOTTI A, YANG Y, SCHMIDT R J, JACKSON D . The relationship between auxin transport and maize branching. Plant Physiology, 2008,147:1913-1923.
[16]	GALLAVOTTI A, ZHAO Q, KYOZUKA J, MEELEY R B, RITTER M K, DOEBLEY J F, PE ME, SCHMIDT R J . The role of barren stalk1 in the architecture of maize. Nature, 2004,432:630-635.
[17]	SKIRPAN A, CULLER A H, GALLAVOTTI A, JACKSON D, COHEN J D, MCSTEEN P . BARREN INFLORESCENCE2 interaction with ZmPIN1a suggests a role in auxin transport during maize inflorescence development. Plant and Cell Physiology, 2009,50:652-657.
[18]	MCSTEEN P, MALCOMBER S, SKIRPAN A, LUNDE C, WU X T, KELLOGG E, HAKE S . Barren inflorescence2 encodes a co-ortholog of the PINOID serine/threonine kinase and is required for organogenesis during inflorescence and vegetative development in maize. Plant Physiology, 2007,144:1000-1011.
[19]	BARAZESH S, MCSTEEN P . Barren inflorescence1 functions in organogenesis during vegetative and inflorescence development in maize. Genetics, 2008,179:389-401.
[20]	GALLI M, LIU Q, MOSS B L, MALCOMBER S, LI W, GAINES C, FEDERICI S, ROSHKOVAN J, MEELEY R, NEMHAUSER J L, GALLAVOTTI A . Auxin signaling modules regulate maize inflorescence architecture. Proceedings of the National Academy of Sciences of the United States of America, 2015,43:13372-13377.
[21]	SKIRPAN A, WU X, MCSTEEN P . Genetic and physical interaction suggest that BARREN STALK1 is a target of BARREN INFLORESCENCE2 in maize inflorescence development. The Plant Journal, 2008,55:787-797.
[22]	PAUTLER M, EVELAND A L, LARUE T, YANG F, WEEKS R, LUNDE C, JE B, MEELEY R, KOMATSU M, VOLLBRECHT E, SAKAI H, JACKSON D . FASCIATED EAR4 encodes a bZIP transcription factor that regulates shoot meristem size in maize. The Plant Cell, 2015,1:104-120.
[23]	YANG F, BUI H T, PAUTLER M, LLACA V, JOHNSTON R, LEE B H, KOLBE A, SAKAI H, JACKSON D . A maize glutaredoxin gene, abphyl2, regulates shoot meristem size and phyllotaxy. The Plant Cell, 2015,27(1):121-131.
[24]	JACKSON D, HAKE S . Control of phyllotaxy in maize by the abphyl1 gene. Development, 1999,126:315-323.
[25]	GIULINI A, WANG J, JACKSON D . Control of phyllotaxy by the cytokinin-inducible response regulator homologue ABPHYL1. Nature, 2004,430:1031-1034.
[26]	JIAO Y, WANG Y, XUE D, WANG J, YAN M, LIU G, DONG G, ZENG D, LU Z, ZHU X, QIAN Q, LI J . Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nature Genetics, 2010,6:541-544.
[27]	MIURA K, IKEDA M, MATSUBARA A, SONG X J, ITO M, ASANO K, MATSUOKA M, KITANO H, ASHIKARI M . OsSPL14 promotes panicle branching and higher grain productivity in rice. Nature Genetics, 2010,6:545-549.
[28]	LIU M, SHI Z, ZHANG X, WANG M, ZHANG L, ZHENG K, LIU J, HU X, DI C, QIAN Q, HE Z, YANG D L . Inducible overexpression of Ideal Plant Architecture1 improves both yield and disease resistance in rice. Nature Plants, 2019,5:389-400.
[29]	SONG X, LU Z, YU H, SHAO G, XIONG J, MENG X, JING Y, LIU G, XIONG G, DUAN J, YAO X, LIU C, LI H, WANG Y, LI J . IPA1 functions as a downstream transcription factor repressed by D53 in strigolactone signaling in rice. Cell Research, 2017,27:1128-1141.
[30]	EVELAND A L, GOLDSHMIDT A, PAUTLER M, MOROHASHI K, LISERON-MONFILS C, LEWIS M W, KUMARI S, HIRAGA S, YANG F, UNGER-WALLACE E, OLSON A, HAKE S, VOLLBRECHT E, GROTEWOLD E, WARE D, JACKSON D . Regulatory modules controlling maize inflorescence architecture. Genome Research, 2014,3:431-443.
[31]	AMBROSE B A, LERNER D R, CICERI P, PADILLA C M, YANOFSKY M F, SCHMIDT R J . Molecular and genetic analyses of the silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Molecular Cell, 2000,5(3):569-579.
[32]	CHENG P C, GREYSON R I, WALDEN D B . Organ initiation and the development of unisexual flowers in the tassel and ear of Zea mays. American Journal of Botany, 1983,70:450-462.
[33]	MENA M, MANDEL M A, LERNER D R, YANOFSKY M F, SCHMIDT R J . A characterization of the MADS-box gene family in maize. The Plant Journal, 1995,8(6):845-854.
[34]	BARTLETT M E, WILLIAMS S K, TAYLOR Z, DEBLASIO S, GOLDSHMIDT A, HALL D H, SCHMIDT R J, JACKSON D P, WHIPPLE C J . The maize PI/GLO ortholog Zmm16/sterile tassel silky ear1 interacts with the zygomorphy and sex determination pathways in flower development. The Plant Cell, 2015,11:3081-3098.
[35]	MÜNSTER T, WINGEN L U, FAIGL W, WERTH S, SAEDLER H, THEISSEN G . Characterization of three GLOBOSA-like MADS-box genes from maize: Evidence for ancient paralogy in one class of floral homeotic B-function genes of grasses. Gene, 2001,262(1/2):1-13.
[36]	SCHMIDT R J, VEIT B, MANDEL M A, MENA M, HAKE S, YANOFSKY M F . Identification and molecular characterization of ZAG1, the maize homolog of the Arabidopsis floral homeotic gene AGAMOUS. The Plant Cell, 1993,5(7):729-737.
[37]	SCHREIBER D N, BANTIN J, DRESSELHAUS T . The MADS box transcription factor ZmMADS2 is required for anther and pollen maturation in maize and accumulates in apoptotic bodies during anther dehiscence. Plant Physiology, 2004,134:1069-1079.
[38]	THEISSEN G, STRATER T, FISHER A, SAEDLER H . Structural characterization, chromosomal localization and phylogenetic evaluation of two pairs of AGAMOUS-like MADS-box genes from maize. Gene, 1995,156(2):155-166.
[39]	MÜNSTER T, DELEU W, WINGEN L U, OUZUNOVA M, CACHARRON J, FAIGL W, WERTH S, KIM J T, SAEDLER H, THEISSEN G . Maize MADS-box genes galore. Maydica, 2002,47:287-301.
[40]	THOMPSON B E, BARTLING L, WHIPPLE C, HALL D H, SAKAI H, SCHMIDT R, HAKE S . Bearded-ear encodes a MADS box transcription factor critical for maize floral development. The Plant Cell, 2009,21(9):2578-2590.
[41]	MENA M, AMBROSE B A, MEELEY R B, BRIGGS S P, YANOFSKY M F, SCHMIDT R J . Diversification of C-function activity in maize flower development. Science, 1996,274(5292):1537-1540.
[42]	CACHARRÓN J, SAEDLER H, THEISSEN G . Expression of MADS-box genes ZMM8 and ZMM14 during inflorescence development of Zea mays discriminates between the upper and the lower floret of each spikelet. Development Genes and Evolution, 1999,209:411-420.
[43]	KOBAYASHI K, MAEKAWA M, MIYAO A, HIROCHIKA H, KYOZUKA J . PANICLE PHYTOMER2 (PAP2), encoding a SEPALLATA subfamily MADS-box protein, positively controls spikelet meristem identity in rice. Nature Reviews Genetics, 2010,511:47-57.
[44]	CIAFFI M, RITA A, ANTONIO O, ENRICO T . Molecular aspects of flower development in grasses. Sexual Plant Reproduction, 2011,24:247-282.
[45]	CHUCK G, MEELEY R B, HAKE S . The control of maize spikelet meristem fate by the APETALA2-like gene indeterminate spikelet1. Genes Development, 1998,12(8):1145-1154.
[46]	CHUCK G, MEELEY R, HAKE S . Floral meristem initiation and meristem cell fate are regulated by the maize AP2 genes ids1 and sid1. Development, 2008,135(18):3013-3019.
[47]	CHUCK G, MEELEY R, IRISH E, SAKAI H, HAKE S . The maize tasselseed4 microRNA controls sex determination and meristem cell fate by targeting Tasselseed6/indeterminate spikelet1. Nature Genetics, 2007,39:1517-1521.
[48]	ACOSTA I F, LAPARRA H, ROMERO S P, SCHMELZ E, HAMBERG M, MOTTINGER J P, MORENO M A, DELLAPORTA S L . tasselseed1 is a lipoxygenase affecting jasmonic acid signaling in sex determination of maize. Science, 2009,323:262-265.
[49]	DELONG A, CALDERON-URREA A, DELLAPORTA S L . Sex determination gene TASSELSEED2 of maize encodes a short-chain alcohol dehydrogenase required for stage-specific floral organ abortion. Cell, 1993,74:757-768.
[50]	YAN Y, CHRISTENSEN S, ISAKEIT T, ENGELBERTH J, MEELEY R, HAYWARD A, EMERY R J N, KOLOMIETS M V . Disruption of OPR7 and OPR8 reveals the versatile functions of jasmonic acid in maize development and defense. The Plant Cell, 2012,24(4):1420-1436.
[51]	LUNDE C, KIMBERLIN A, LEIBOFF S, KOO A J, HAKE S . Tasselseed5 overexpresses a wound-inducible enzyme, ZmCYP94B1, that affects jasmonate catabolism, sex determination, and plant architecture in maize. Communications Biology, 2019,2:114.
[52]	HAYWARD A P, MORENO M A, HOWARD T P, HAGUE J, NELSON K, HEFFELFINGER C, ROMERO S, KAUSCH A P, GLAUSER G, ACOSTA I F, ET A L . Control of sexuality by the sk1-encoded UDP-glycosyltransferase of maize. Science Advances, 2016,2:e1600991.
[53]	IRISH E E, LANGDALE J A, NELSON T M . Interactions between tassel seed genes and other sex determining genes in maize. Developmental Genetics, 1994,15:155-171.
[54]	HARTWIG T, CHUCK G S, FUJIOKA S, KLEMPIEN A, WEIZBAUER R, POTLURI D P V, CHOE S, JOHAL G S, SCHULZ B . Brassinosteroid control of sex determination in maize. Proceedings of the National Academy of Sciences of the United States of America, 2011,108(49):19814-19819.
[55]	BEST N B, HARTWIG T, BUDKA J, FUJIOKA S, JOHAL G, SCHULZ B, DILKES B P . nana plant2 encodes a maize ortholog of the Arabidopsis brassinosteroid biosynthesis protein Dwarf1, identifying developmental interactions between brassinosteroids and gibberellins. Plant Physiology, 2016,171:2633-2647.
[56]	HABBEN J E, BAO X, BATE N J, DEBRUIN J L, DOLAN D, HASEGAWA D, HELENTJARIS T G, LAFITTE R H, LOVAN N, MO H, REIMANN K, SCHUSSLER J R . Transgenic alteration of ethylene biosynthesis increases grain yield in maize under field drought-stress conditions. Plant Biotechnology Journal, 2014,12:685-693.
[57]	SHI J, HABBEN J E, ARCHIBALD R L, DRUMMOND B J, CHAMBERLIN M A, WILLIAMS R W, LAFITTE H R, WEERS B P . Overexpression of ARGOS genes modifies plant sensitivity to ethylene, leading to improved drought tolerance in both Arabidopsis and maize. Plant Physiology, 2015,169(1):266-282.
[58]	SCANLON M J, TAKACS E M. Kernel biology//BENNETZEN J, HAKE S, eds.,Handbook of Maize: Its Biology. New York: Springer Press, 2009: 121-143.
[59]	LI X J, ZHANG Y F, HOU M, SUN F, SHEN Y, XIU Z H, WANG X, CHEN Z L, SUN S S, SMALL I, TAN B C . Small kernel 1 encodes a pentatricopeptide repeat protein required for mitochondrial nad7 transcript editing and seed development in maize (Zea mays) and rice (Oryza sativa). The Plant Journal, 2014,79(5):797-809.
[60]	YANG Y Z, DING S, WANG Y, LI C L, SHEN Y, MEELEY R . Small kernel2 encodes a glutaminase in vitamin B6 biosynthesis essential for maize seed development. Plant Physiology, 2017,174(2):1127-1138.
[61]	NEUFFER M G, SHERIDAN W F . Defective kernel mutants of maize: I. Genetic and lethality studies. Genetics, 1980,95(4):929-944.
[62]	SCANLON M J, STINARD P S, JAMES M G, MYERS A M, ROBERTSON D S . Genetic analysis of 63 mutations affecting maize kernel development isolated from Mutator stocks. Genetics, 1994,136(1):281-294.
[63]	FU S, MEELEY R, SCANLON M J . Empty pericarp2 encodes a negative regulator of the heat shock response and is required for maize embryogenesis. The Plant Cell, 2002,14(12):3119-3132.
[64]	HECKEL T, WERNER K, SHERIDAN W F, DUMAS C, ROGOWSKY P M . Novel phenotypes and developmental arrest in early embryo specific mutants of maize. Planta, 1999,210(1):1-8.
[65]	SHEN Y, LI C, MCCARTY D R, MEELEY R, TAN B C . Embryo defective12 encodes the plastid initiation factor 3 and is essential for embryogenesis in maize. The Plant Journal, 2013,74(5):792-804.
[66]	QI W, YANG Y, FENG X, ZHANG M, SONG R . Mitochondrial function and maize kernel development requires dek2, a pentatricopeptide repeat protein involved in nad1 mRNA splicing. Genetics, 2017,205(1):239-249.
[67]	CHEN X, FENG F, QI W, XU L, YAO D, WANG Q , SONG R. dek35 encodes a PPR protein that affects cis-splicing of mitochondrial nad4 intron 1 and seed development in maize. Molecular Plant, 2017,10(3):427-441.
[68]	DAI D, LUAN S, CHEN X, WANG Q, FENG Y, ZHU C, QI W, SONG R . Maize dek37 encodes a p-type PPR protein that affects cis-splicing of mitochondrial nad2 intron 1 and seed development. Genetics, 2018,208(3):1069-1082.
[69]	QI W, TIAN Z, LU L, CHEN X, CHEN X, ZHANG W, SONG R . Editing of mitochondrial transcripts nad3 and cox2 by dek10 is essential for mitochondrial function and maize plant development. Genetics, 2017,205(4):1489-1501.
[70]	WANG G, ZHONG M, SHUAI B, SONG J, ZHANG J, HAN L, LING H, TANG Y, WANG G, SONG R . E+ subgroup PPR protein Defective Kernel 36 is required for multiple mitochondrial transcripts editing and seed development in maize and Arabidopsis. New Phytologist, 2017,214(4):1563-1578.
[71]	LI X, GU W, SUN S, CHEN Z, CHEN J, SONG W, ZHAO H, LAI J . Defective Kernel 39 encodes a PPR protein required for seed development in maize. Journal of Integrative Plant Biology, 2018,60(1):45-64.
[72]	SUN F, ZHANG X, SHEN Y, WANG H, LIU R, WANG X, GAO D, YANG Y Z, LIU Y, TAN B C . The pentatricopeptide repeat protein EMPTY PERICARP8 is required for the splicing of three mitochondrial introns and seed development in maize. The Plant Journal, 2018,95:919-932.
[73]	CAI M, LI S, SUN F, SUN Q, ZHAO H, REN X, ZHAO Y, TAN B C, ZHANG Z, QIU F . Emp10 encodes a mitochondrial PPR protein that affects the cis-splicing of nad2 intron 1 and seed development in maize. The Plant Journal, 2017,91(1):132-144.
[74]	REN X, PAN Z, ZHAO H, ZHAO J, CAI M, LI J, ZHANG Z, QIU F . EMPTY PERICARP11 serves as a factor for splicing of mitochondrial nad1 intron and is required to ensure proper seed development in maize. Journal of Experimental Botany, 2017,68(16):4571-4581.
[75]	SUN F, XIU Z, JIANG R, LIU Y, ZHANG X, YANG Y Z, LI X, ZHANG X, WANG Y, TAN B C . The mitochondrial pentatricopeptide repeat protein EMP12 is involved in the splicing of three nad2 introns and seed development in maize. Journal of Experimental Botany, 2019,70(3):963-972.
[76]	XIU Z, SUN F, SHEN Y, ZHANG X, JIANG R, BONNARD G, ZHANG J, TAN B C . EMPTY PERICARP16 is required for mitochondrial nad2 intron 4 cis-splicing, complex I assembly and seed development in maize. The Plant Journal, 2016,85(4):507-519.
[77]	LIU Y J, XIU Z H, MEELEY R, TAN B C . Empty pericarp5 encodes a pentatricopeptide repeat protein that is required for mitochondrial RNA editing and seed development in maize. The Plant Cell, 2013,25(3):868-883.
[78]	SUN F, WANG X, BONNARD G, SHEN Y, XIU Z, LI X, GAO D, ZHANG Z, TAN B C . Empty pericarp7 encodes a mitochondrial E-subgroup pentatricopeptide repeat protein that is required for ccmFN editing, mitochondrial function and seed development in maize. The Plant Journal, 2015,84(2):283-295.
[79]	YANG Y Z, DING S, WANG H C, SUN F, HUANG W L, SONG S, XU C, TAN B C . The pentatricopeptide repeat protein EMP9 is required for mitochondrial ccmB and rps4 transcript editing, mitochondrial complex biogenesis and seed development in maize. New Phytologist, 2017,214(2):782-795.
[80]	LI X L, HUANG W L, YANG H H, JIANG R C, SUN F, WANG H C, ZHAO J, XU C H, TAN B C . EMP18 functions in mitochondrial atp6 and cox2 transcript editing and is essential to seed development in maize. New Phytologist, 2019,221(2):896-907.
[81]	GUTIERREZ-MARCOS J F, DAL PRA M, GIULINI A, COSTA L M, GAVAZZI G, CORDELIER S, SELLAM O, TATOUT C, PAUL W, PEREZ P, DICKINSON H G, CONSONNI G . Empty pericarp4 encodes a mitochondrion-targeted pentatricopeptide repeat protein necessary for seed development and plant growth in maize. The Plant Cell, 2007,19(1):196-210.
[82]	OFFLER C E, MCCURDY D W, PATRICK J W, TALBOT M J . Transfer cells: Cells specialized for a special purpose. Annual Review of Plant Biology, 2003,54:431-454.
[83]	BRYANT N, LLOYD J, SWEENEY C, MYOUGA F, MEINKE D . Identification of nuclear genes encoding chloroplast-localized proteins required for embryo development in Arabidopsis. Plant Physiology, 2011,155(4):1678-1689.
[84]	SOSSO D, CANUT M, GENDROT G, DEDIEU A, CHAMBRIER P, BARKAN A, CONSONNI G, ROGOWSKY P M . PPR8522 encodes a chloroplast-targeted pentatricopeptide repeat protein necessary for maize embryogenesis and vegetative development. Journal of Experimental Botany, 2012,63(16):5843-6857.
[85]	LI C, SHEN Y, MEELEY R, MCCARTY D R, TAN B C . Embryo defective 14 encodes a plastid-targeted cGTPase essential for embryogenesis in maize. The Plant Journal, 2015,84(4):785-799.
[86]	ZHANG Y F, HOU M M, TAN B C . The requirement of WHIRLY1 for embryogenesis is dependent on genetic background in maize. PLoS ONE, 2013,8(6):e67369.
[87]	MA Z, DOONER H K . A mutation in the nuclear-encoded plastid ribosomal protein S9 leads to early embryo lethality in maize. The Plant Journal, 2004,37(1):92-103.
[88]	LI Q, WANG J, YE J, ZHENG X, XIANG X, LI C, FU M, WANG Q, ZHANG Z, WU Y . The maize imprinted gene Floury3 encodes a PLATZ protein required for tRNA and 5S rRNA transcription through interaction with RNA Polymerase III. The Plant Cell, 2017,29(10):2661-2675.
[89]	LI J, FU J, CHEN Y, FAN K, HE C, ZHANG Z, LI L, LIU Y, ZHENG J, REN D, WANG G . The U6 Biogenesis-Like 1 plays an important role in maize kernel and seedling development by affecting the 3' end processing of U6 snRNA. Molecular Plant, 2017,10(3):470-482.
[90]	ZUO Y, FENG F, QI W, SONG R . Dek42 encodes an RNA-binding protein that affects alternative pre-mRNA splicing and maize kernel development. Journal of Integrative Plant Biology, 2019,61(6):728-748
[91]	WANG H, WANG K, DU Q, WANG Y, FU Z, GUO Z, KANG D, LI W X, TANG J . Maize Urb2 protein is required for kernel development and vegetative growth by affecting pre-ribosomal RNA processing. New Phytologist, 2018,218(3):1233-1246.
[92]	HE Y, WANG J, QI W, SONG R . Maize Dek15 encodes the Cohesin- Loading Complex Subunit SCC4 and is essential for chromosome aegregation and kernel development. The Plant Cell, 2019,31(2):465-485.