赵然, 蔡曼君, 杜艳芳, 张祖新^,华中农业大学作物遗传改良国家重点实验室,武汉 430070

Molecular Basis of Kernel Development and Kernel Number in Maize (Zea mays L.)

ZHAO Ran, CAI ManJun, DU YanFang, ZHANG ZuXin^,National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan 430070

通讯作者: 张祖新,E-mail：zuxinzhang@mail.hzau.edu.cn

责任编辑: 李莉
收稿日期:2019-04-17接受日期:2019-06-20网络出版日期:2019-10-16

基金资助:

国家自然科学基金.31871628

Received:2019-04-17Accepted:2019-06-20Online:2019-10-16
作者简介 About authors
赵然,E-mail：zhaoran@webmail.hzau.edu.cn






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.
Keywords：Zea mays L.;kernel number per ear;kernel weight;inflorescence;floret;embryo;endosperm


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本文引用格式
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 doi:10.3864/j.issn.0578-1752.2019.20.001
ZHAO Ran, CAI ManJun, DU YanFang, ZHANG ZuXin. Molecular Basis of Kernel Development and Kernel Number in Maize (Zea mays L.)[J]. Scientia Acricultura Sinica, 2019, 52(20): 3495-3506 doi:10.3864/j.issn.0578-1752.2019.20.001

0 引言

玉米（Zea mays L.）籽粒是重要的粮食、饲料、工业和能源原料,在保障粮食安全、经济发展及缓解能源危机等方面起重要作用。因而,玉米籽粒产量形成的生物学基础解析吸引了许多科学家的关注,成为遗传学、发育生物学和作物育种学等学科的重大科学问题。随着群体遗传学、基因组学、发育生物学和分子生物学等学科的理论和技术发展及其在玉米研究中的应用,玉米籽粒产量及其相关性状形成的生物学基础等研究领域取得了重要进展。由于玉米单穗籽粒产量由穗粒数和粒重两个因子组成,本文将主要围绕穗粒数和粒重发育相关基因及其调控网络,简要介绍国内外在这一领域所取得的主要成果。

1 穗粒数与雌花序发育

玉米果穗是雌花序上各类分生组织按其固有模式分化和发育的最终结果。花序分生组织（inflorescence meristem,IM）产生数目不等的成对小穗分生组织（spikelet-paired meristem,SPM）,而每个SPM进一步分化出2个小穗分生组织（spikelet meristem,SM）,随着小花分生组织（floral meristem,FM）的产生,花序分化终止,这一过程称之为花序发育;FM经花器官分化和发育形成小花,这一过程称之为小花发育^[1]。授粉后,小花经胚和胚乳发育形成籽粒。由此可见,花序和小花中各类分生组织的正常起始和发育与花序上最终形成的小花数目和每穗籽粒数密切相关。由于花序建成和小花发育是籽粒产量的生物学基础,因而,这一研究领域吸引了许多科学家的关注。目前,对玉米花序建成和小花发育调控的认知主要来自于对突变体的深入分析。已鉴定的控制花序上各类分生组织分化和花器官发育的基因分别参与了以下几条调控途径。

1.1 CLAVATA-WUSCHEL（CLV-WUS）负反馈调控途径

参与该途径的基因,通过调控分生组织中干细胞分裂和分化的平衡,维系干细胞数目并源源不断产生新的组织或器官^[2,3]。玉米中参与该途径的基因包含：分别编码拟南芥CLAVATA1（CLV1）、CLV2和CLV3同源蛋白的基因THICK TASSEL DWARF1（TD1）^[4]、FASCIATED EAR2（FEA2）^[5]和FEA3^[6],编码CLV3/EMBRYO-SURROUNDING REGION（CLE）类信号肽分子的基因FON2-LIKE CLE PROTEIN1（FCP1）、ZmCLE7和ZmCLE14^[6,7],以及编码下游效应分子的基因COMPACT PLANT2（CT2）^[8]和Zea mays CORYNE（ZmCRN）等^[9]。这一途径中各基因间的相互关系已有许多综述,不再赘述,仅以图1作简单描述（图1）。与拟南芥中形成受体复合体不同,玉米TD1和FEA2可能在不同的遗传途径发挥作用。

图1

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图1雌花序上各分生组织活性调控基因的表达位置及调控途径

图片显示的是玉米雌花序分生组织和成对小穗分生组织的原基。不同颜色块表示基因表达的组织部位或组织。 表示正调控。 表示负调控
Fig. 1Expression domain and regulatory pathway of genes involved in the regulation of activity of meristems on the ear inflorescence

The figure shows the ear inflorescence meristem and primordia of spikelet-paired meristems. Different color blocks show the domains where genes are expressed.: Positive regulation. : Negative regulation


近年来研究证实,编码SQUAMOSA promoter binding protein（SBP）转录因子的UNBRANCHED2（UB2）和UB3也参与花序分生组织活性的调控。UB2和UB3主要在SPM的外缘表达,ub2或ub3单突变体的花序无明显异常表型,而ub2ub3双突变体的雌花序分化提前终止、顶部异常膨大、穗行数增加、果穗变短,显示出这两个基因功能的部分冗余^[10]。过表达UB2或UB3的植株其花序分化也受到抑制并提前终止、花序变短、穗粒数减少。同时,UB3也是GIF1（GROWTH-REGULATING FACTOR（GRF）-INTERACTING FACTOR 1）的靶基因,其表达受GIF1调控。功能丧失突变体gif1也表现出与ub2ub3双突变体相似的花序膨大表型^[11]。其次,UB3还可结合到LONELY GUY1（LOG1）和TYPE-A RESPONSE REGULATOR（ARR）启动子,调控LOG1和ARR的表达,进而参与细胞分裂素（CKs）合成和信号途径^[12]。另外,UB3也可通过调控FCP1和ZmWUS1参与到CLV-WUS途径来调节花序分生组织的大小和小穗原基的起始,从而调控穗行数^[12]。这些研究描绘了一条以UB3为中心调控花序发育的新途径,即GIF1正调控UB3,而UB3负调控FCP1,通过FCP1连接CLV-WUS途径（图1）。

尽管玉米CLV-WUS途径中关键基因的强突变导致雌穗顶端扁平、穗行数增加、穗长变短、单穗籽粒产量下降,但是,fea2和fea3弱等位突变能维持分生组织正常发育,并通过增加IM大小和SPM原基起始数目来增加穗行数,最终导致穗粒数增加,提高了单穗籽粒产量^[6,8]。而在自交系群体中,UB3编码区的一个A/G变异引起第220位的丝氨酸变为天冬酰胺,该变异位点与穗行数关联^[10]。另外,在UB3下游约60 kb位置,有一个主效QTL KRN4。KRN4为一段非编码DNA,其中一个转座子片段的插入/缺失可调节UB3的表达水平,进而导致穗行数的数量变异^[13]。这些研究说明,玉米花序发育关键基因的弱突变可以引起籽粒产量相关性状的数量变异,基因组上非编码区的变异也可通过调节花序发育关键基因的表达水平,进而引起籽粒产量相关性状的数量变异。

1.2 激素及其信号途径

植物激素及其信号也参与雌花序上各类分生组织的确定性和活性的调控。这些基因基于其作用途径大致分为：1）生长素合成及其信号相关基因。这些基因包括生长素合成相关基因VANISHING TASSEL2（VT2）和SPARSE INFLORESCENCE1（SPI1）（图2-a）、生长素运输和定位相关基因BARREN INFLORESCENCE2（BIF2）、生长素信号相关基因BIF1、BIF4和FEA4（图2-b）。VT2编码色氨酸氨基转移酶,催化色氨酸向吲哚-3-丙酮酸的转变^[14];SPI1编码一个单子叶植物特有的黄素单加氧酶^[15]。vt2和spi1突变体均表现为雌雄花序上IM分化活性下降、各类次生分生组织分化受到抑制、花序分化提前终止、小花数目明显减少^[14]。BIF2编码一个与拟南芥PINOID同源的丝氨酸/苏氨酸蛋白激酶,可与Zea mays PIN-FORMED1a（ZmPIN1a）和一个bHLH转录因子BARREN STALK1（BA1）互作^[16,17],参与生长素极性运输。突变体bif2雌雄穗分枝难以分化,小穗分生组织减少^[18]。可见,BIF2主要参与IM分化和SPM活性维持。另外,BIF1和BIF4均编码生长素信号途径的AUX/IAA蛋白,其突变体表现为与bif2相似的表型,雌雄穗分枝数和小花数均受到严重抑制^[19,20]。而ba1突变体无雌穗、且雄穗无分支和小穗,表明BA1在营养和生殖发育中调节次生分生组织的起始;BA1的这些功能受BIF1、BIF2和BIF4的调控^[20,21]。除此之外,FEA4编码一个bZIP转录因子,通过调控生长素响应因子（ARF）参与生长素信号途径、进而调控雌花序SPM的确定性^[22]。而MALE STERILE CONVERTED ANTHER1（MSCA1）编码的谷氧还蛋白（GRX）能与FEA4互作,形成MSCA1-FEA4-ARF的生长素信号调控途径^[23]。因此,在玉米中可通过影响生长素合成、运输及信号相关基因,调控花序发育,进而影响籽粒产量。2）激素交互作用的关键基因。ABERRANT PHYLLOTAXY1（ABPH1）编码一个CKs诱导的类型A响应调节子,在拟南芥中可正调控生长素信号、负调控细胞分裂素信号^[24]。在玉米abph1突变体中,生长素水平和PIN1的表达均降低,导致茎顶端分生组织（shoot apical meristem,SAM）膨大,叶原基起始推迟,说明在玉米SAM中ABPH1也是生长素水平和运输的正调控因子,揭示了组织和器官发生过程中植物激素平衡调节的重要性^[25]。UB3是水稻重要株型和产量基因IDEAL PLANT ARCHITECTURE1（IPA1）的同源基因^[26,27]。在水稻中,IPA1既可与赤霉素（GAs）抑制因子DELLA蛋白互作干扰DELLA蛋白的降解,抑制赤霉素信号转导^[28],又与独脚金内酯（SL）信号通路中的关键负调控因子Dwarf 53（D53）蛋白直接互作抑制IPA1的转录激活活性;IPA1还能直接结合D53的启动子并激活D53的表达,形成负反馈调节^[29]。然而,UB3/IPA1在水稻中的这一负反馈调节途径在玉米中是否存在还有待进一步研究。不过,玉米UB3在水稻表达中则参与了CKs的合成和信号途径,进而调控分支分生组织的起始^[12],由此可见,UB3/IPA1参与多种激素信号途径,可能是一个连接激素信号和CLV-WUS途径的关键因子。随着测序技术的发展,基于转录组学分析揭示了CKs和GAs在玉米花序发育中的作用及其调控关系,发现RAMOSA1（RA1）和KNOTTED1（KN1）可能参与GA合成和信号途径：即RA1结合D1（ZmGA3ox2）正调控D1表达,也负调控GA信号抑制子SPY（ZmGA2ox1）,时空特异性地激活GA合成和代谢相关基因进而调控GA水平,而KN1和SPY则能正调控CKs^[30]（图2-c）。这些结果说明了花序建成和发育中激素作用的重要性和复杂性。

图2

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图2激素及其信号相关基因调控花序上分生组织活性的途径

a：SPI1和VT2调控色氨酸依赖的生长素合成。b：生长素转运与信号相关基因及其调控途径。c：UB3介导的激素交互作用。 表示正调控。 表示负调控
Fig. 2Regulation pathways for activity of meristems on the ear inflorescence by genes in hormone biosynthesis and signaling

a: Both SPI1 and VT2 involve in the regulation of Trp-dependent auxin biosynthesis. b: Regulatory pathways of genes in auxin transport and signaling. c: Presumable hormone crosstalk mediated by UB3. : Positive regulation. : Negative regulation

2 穗粒数与小花发育

在发育生物学上,玉米穗粒数是穗行数与行粒数的集合。它们的形成需经历花序形态建成和小花发育2个过程,前者决定花序上所分化的小花数目,后者决定小花育性和授粉结实潜力。而小花分生组织分化产生的花器官分生组织及其有序性地发育是小花发育的主要生物学事件,因此,花器官分生组织的起始和发育也与穗粒数密切相关。玉米雌、雄小花分生组织均能分化出1个外稃、1个内稃、2个浆片、3个雄蕊和3个心皮原基,其中,内外稃等同于双子叶植物花的萼片,浆片等同于花瓣,说明玉米花器官发育也遵循“ABCDE”模型^[31]。尽管每朵玉米小花均能分化出两性花所具有的花器官原基,但成熟的玉米小花仍发育成为单性花,即雄花中心皮发育被抑制、而雌花中雄蕊发育被抑制^[32],形成了同一小花中雌蕊或雄蕊选择性发育的特征。这一特征也是玉米与其他禾谷类作物及模式植物拟南芥在小花发育调控上的区别,使得玉米小花成为花器官发育研究的理想材料。

迄今为止,在玉米中所鉴定到的花器官发育相关基因,主要包含1个A类基因Zea APETALA Homolog1（ZAP1）^[33],4个B类基因SILKY1（SI1）^[31]、Zea mays MADS16 （ZMM16）/STERILE TASSEL SILKY EAR1（STS1）^[34]、ZMM18和ZMM29^[35],3个C类基因Zea AGAMOUS1（ZAG1）^[36]、ZMM2^[37]和ZMM23^[38],3个D类基因ZAG2^[36]、ZMM1^[38]和ZMM25^[38],以及4个E类基因ZAG3/BEARDED-EAR（BDE）^[40]、ZAG5^[41]、ZMM8和ZMM14^[42,43,44]（图3-a）,其中,仅有SI1、ZMM16和BDE的功能解析最清楚。SI1在雄蕊和浆片中特异表达,其突变后导致雄蕊转换为心皮、浆片转换为类似于内外稃的结构,因而,si1突变体表现为雄性不育^[31]。ZMM16与拟南芥B类基因APETALA3/ DEFICIENS同源,在雄蕊原基、雄蕊和浆片中特异表达。在zmm16自然突变体中,雄花浆片和雄蕊转变成内外稃、雌花中本应退化的雄蕊转变成心皮,雌、雄小花均不育^[34]。BDE在小花分生组织、浆片、心皮原基和内稃中均有表达,在内珠被和胚珠原基表达水平最高。BDE蛋白可与ZAG1互作调控小花分生组织的产生和花器官分生组织的起始与活性维持。在bde突变体中,雄花产生额外的花器官、雄蕊发育受到部分抑制、而雌蕊发育异常激活而形成花丝,雌花产生内外稃的结构、一个胚珠上生长出多个花丝^[40]。这些“ABCDE”模型中的同源基因,由于直接调节花器官的发育而影响小花的育性,因此也影响授粉后果穗上的籽粒数。

图3

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图3调控玉米花器官发育和小花性别决定的基因

a：玉米花器官发育“ABCDE”模型调控基因。不同色块代表不同类型的花器官调控基因,下方标注代表不同花器官及其对应轮数。A类基因决定第一轮内稃和外稃的形成,第二轮和第三轮浆片和雄蕊的形成分别由A+B和B+C基因调控,第四轮心皮发育则由C类基因单独调控。D类基因主要在胚珠发育中起作用,E类基因则参与所有的花器官发育调控。b：小花性别决定基因调控网络。 表示正调控。 表示负调控
Fig. 3Genes regulating maize floral organs development and floret sex determination

a: The “ABCDE model” of floral organ identity. Different color blocks show different types of floral organ regulatory genes, and the label shows floral organ developed in the whorl. A-type genes determine the identity of palea and lemma. Lodicule and stamen are regulated by A+B and B+C, respectively. Carpel identity is regulated by the C-type genes. D-type genes act in ovule development, and the E-type genes involve in the regulation of development of all floral whirls. b: Floret sex determination genes regulatory network. : Positive regulation. : Negative regulation


除“ABCDE”花器官发育模型相关基因外,对玉米雌、雄性器官选择性发育的调控研究,丰富了对植物小花性别决定的认识。控制分生组织确定性的基因在性别决定中扮演重要角色。TASSELSEED6（TS6）/INDETERMINATE SPIKELET1（IDS1）编码APETALA2（AP2）/ERF转录因子,突变体ts6/ids1的小穗分生组织确定性丧失,产生额外小花,并且雄花序部分小花因心皮发育产生花丝^[45],与其功能相似的同源基因SISTER OF INDETERMINATE SPIKELET1（SID1）则具有积加效应^[46]。而TS4编码的miR172靶向TS6/IDS1和SID1,负调控它们的表达^[47]（图3-b）。另外,研究发现茉莉酸（JAs）和油菜素内酯（BRs）可通过调控小花的性别进而调节小花育性和授粉潜力。目前,玉米中已克隆了6个JAs合成和代谢相关基因,其中,TS1编码一个脂氧化酶^[48]、TS2编码一种单子叶植物所特有的短链乙醇脱氢酶^[49],OPR7和OPR8是2个同源基因,均编码12-氧-植物二烯酸还原酶（12-oxo-phytodienoic acid reductase）^[50],这4个基因共同参与JA的生物合成。单突变体ts1、ts2和双突变体opr7opr8均影响JA生物合成,导致JA水平下降,雄穗上部分小花产生花丝^[47,48,49]。显性Ts5突变体的雄花序上也发育出雌性小花、产生花丝。TS5编码一个ZmCYP94B1蛋白,参与JA代谢,即负调控JA水平^[51]（图3-b）。由此可见,高水平的JA是玉米雄花中雌蕊退化或者抑制心皮发育所必要的。那么,玉米雌花中控制雄蕊退化或者保持雌蕊发育的关键基因是什么?SK1编码一个尿苷二磷酸糖基转移酶,该酶可阻断JA生物合成;在sk1突变体中,其雄穗发育正常、但雌穗花丝发育受到抑制^[52]。sk1ts2双突变体雌穗花丝恢复,而雄穗大多数小花也能发育雄蕊^[53];而sk1Ts5双突变体的雌穗无花丝,雄穗产生少量花丝^[51]。结果表明,SK1是雌花中雌蕊发育所必需的,并且阻断JA合成有利于雌蕊发育。除了JA外,BR也在玉米小花性别决定中起着重要作用。例如,NANA PLANT1（NA1）是一个BR生物合成途径的酶编码基因,在花药发育整个过程中均有表达、也在心皮原基表层细胞中表达直至其退化;na1突变体的雄穗部分小花花药退化而花丝发育,并有类似内外稃的变形叶,成熟植株的雄穗上着生有种子,突变体的雌穗和雌花发育正常^[54]。NANA PLANT2（NA2）也参与BR生物合成途径,其突变体表现为与na1相似的表型^[55]。这说明BR在雄蕊和雌蕊发育中起着不同作用,即BR促进雄蕊发育而抑制心皮分生组织的分化,而调节BR在玉米雌花和雄花发育中不同功能的机理至今未知。

近年来,沉默乙烯合成途径的1-Aminocyclopropane- 1-Carboxylase Synthase6（ACS6）,能增加转基因玉米家系在缺水和低氮条件下的产量^[56];过表达乙烯信号途径的组分AUXIN-REGULATED GENE INVOLVED IN ORGAN SIZE（ARGOS）可增加转基因家系和杂交种在正常和干旱条件下的穗长、穗粒数及籽粒产量^[57]。结果表明,乙烯水平和信号或直接参与花序和小花发育、或通过参与玉米对胁迫的响应间接地影响花序和小花发育。这些发现也指出一条“通过调控乙烯合成和信号进而提高玉米抗性和籽粒产量”的新途径。

3 胚和胚乳发育

玉米籽粒由来自母本的种皮、经双受精产生的二倍体胚和三倍体胚乳3种组织组成^[58],其中,胚和胚乳分别占成熟籽粒重量的8%—10%和80%—85%,可见,胚和胚乳发育直接影响籽粒大小和粒重。

为研究胚和胚乳发育的遗传调控,科学家鉴定到了许多胚和胚乳发育突变体,并将这些突变体命名为small kernel（smk）^[59,60]或defective kernel（dek）^[61,62]或empty pericarp（emp）^[63]。其中,emp突变体是dek中极端表型类型,其胚和胚乳发育严重迟滞,成熟突变籽粒被正常籽粒挤压成纸片状^[63]。另外,与emp不同,embryo-specific（emb）突变体影响胚形态建成,导致籽粒不能正常萌发,胚乳可正常发育但籽粒变小^[64,65]。近年来,一批突变体基因的鉴定与分离,从而对玉米胚和胚乳发育的遗传基础有了一个较为系统的认识。

3.1 线粒体基因转录本的加工和编辑与胚和胚乳发育

在已克隆的籽粒发育突变体中,大多数基因编码PPR蛋白家族成员。已克隆的6个DEK基因编码线粒体靶向的PPR蛋白,分别参与线粒体基因内含子剪切（DEK2^[66]、DEK35^[67]、DEK37^[68]）或RNA编辑（DEK10^[69]、DEK36^[70]和DEK39^[71]）。同样,已克隆的12个emp突变体基因中,10个编码线粒体靶向的PPR蛋白,分别参与内含子剪切（EMP8^[72]、 EMP10^[73]、EMP11^[74]、EMP12^[75]和EMP16^[76]）、RNA编辑（EMP5^[77]、EMP7^[78]、EMP9^[79]和EMP18^[80]）和线粒体转录本的表达调控（EMP4^[81]）。此外,SMK1也编码1个PPR蛋白,其功能为线粒体NAD7转录后的编辑^[59]。这些突变体的线粒体电子传递链复合体不能正常组装,导致电子传递、ATP合成受阻,因而,这些基因突变后会强烈影响胚乳细胞发育这个十分耗能的进程^[82],同时也说明玉米胚和胚乳发育依赖于PPR蛋白靶向线粒体基因的转录后加工。

3.2 质体基因的转录和翻译与胚发育

在拟南芥中,30%的胚发育突变体由质体靶向蛋白的功能异常所引起^[83],在一定程度上说明质体在胚形态建成过程中扮演举足轻重的角色。在玉米中,影响胚发育的emb也编码质体靶向蛋白,并通过不同的途径影响胚发育。如EMB2/PPR8522编码一个PPR蛋白,PPR8522可能通过与靶向质体的σ因子（SIG6）互作,影响依赖于质体编码的RNA polymerase进行转录的基因表达,进而影响类囊体结构导致胚致死^[84]。EMB12编码质体起始因子IF3,影响质体蛋白的合成^[65]。EMB14编码一个GTP酶,功能缺失后降低16S rRNA和质体核糖体基因的表达,影响核糖体组装,最终影响质体蛋白翻译^[85]。EMB16编码DNA/RNA结合蛋白WHIRLY1（WHY1）,该蛋白在稳定质体基因组及核糖体形成过程中起着重要作用^[86]。另外,lem1编码一个质体核糖体蛋白PRPS9（plastid 30S ribosomal protein S9）,与EMB一样,其功能缺失只影响胚的发育^[87]。结果表明,质体也在维持玉米胚发育过程中起着必不可少的作用。

3.4 籽粒发育与细胞核RNA转录和加工

近年来,从所分离的几个突变体基因中了解玉米籽粒发育遗传调控的新途径。如FLOURY3（FL3）编码一个PLATZ（plant AT-rich sequence and zinc binding）家族蛋白,该蛋白可与RNA聚合酶Ⅲ的2个亚基结合,调控tRNA和5S rRNA转录。由于FL3只在淀粉胚乳细胞中表达,其突变后特异影响胚乳发育^[88]。UBL1编码一个RNA外切酶,通过影响U6 snRNA 3′-末端的加工,导致前体mRNAs剪切异常,最终影响籽粒和植株发育^[89]。DEK42编码RRM_RBM48型RNA结合蛋白,与其他剪接体组分相互作用参与前体mRNA剪接调节,它的突变显著改变表达基因的选择性剪接,使得U12型内含子被保留于转录本中,表现出小粒和幼苗致死表型^[90]。而Urb2作用于前体rRNA加工,在urb2突变体中,前体rRNA中间产物显著富集,很多核糖体相关基因的表达水平也受到影响,籽粒发育和植株生长都受到抑制^[87]。结果表明,这些基因直接参与到了细胞核内mRNA或者rRNA加工这一基础生物学过程,因此,细胞核RNA转录加工对籽粒发育有着深远影响^[91]。此外,DEK15则编码SISTER CHROMATID COHESION PROTEIN 4（SCC4）的同系物,dek15突变可破坏有丝分裂细胞周期和核内复制,导致胚乳和胚胎致死^[92]。这项新的发现揭示了玉米有丝分裂染色体分离和内核发育的异常,也可导致籽粒发育缺陷。由于上述基因参与许多生物学过程的调控,这些基因突变常会影响包含籽粒发育在内的、广泛的生物学性状,显示出基因功能的多效性。

4 展望

基于突变体的遗传分析,科学家已鉴定并分离了一批玉米花序、小花和籽粒发育相关基因,对许多基因的作用机理和调控途径有了深入研究,但相较于模式植物拟南芥和模式作物水稻,玉米中所克隆的基因数目相对较少,而直接控制穗粒数和粒重的基因数目更少。为深入解析玉米产量及产量相关性状形成的生物学基础,进一步鉴定并克隆更多新的产量及产量相关性状的基因、阐明多基因之间的互作关系、挖掘控制产量相关性状的关键节点基因并解析其调控网络、探究发育相关基因的自然变异与产量及产量相关性状的关系等,将是今后一定时期内玉米遗传学研究的重点和热点领域。玉米籽粒着生于雌穗,雌穗上所形成的籽粒其实质是花序和小花中各类分生组织起始、分化和发育以及授粉后的籽粒发育等生物学过程的最终结果。经长期研究已鉴定到了一批花序和小花发育相关的基因,特别是鉴定到了许多参与CLV-WUS负反馈途径、“ABCDE”模型及激素合成和信号途径等的关键基因,并对这些基因在玉米花序和小花发育中的生物学功能和作用机理与其在拟南芥、水稻中的保守性和差异性进行了分析。但是,各类分生组织起始、分化和终止的内外信号、CLV-WUS途径调控干细胞增殖和分化的上下游基因及其精细调控网络、小花性别分化的遗传控制、激素及其交互作用调控花器官特别是雄蕊和心皮分化和发育的分子途径等研究尚浅,将是玉米发育生物学重点研究领域。在籽粒发育这一研究领域,将进一步鉴定胚和胚乳发育新基因和新调控途径,重点发掘发育相关基因与粒重的关联,揭示其自然变异,为粒重遗传改良提供基因资源。另外,穗粒数、粒型和粒重等也是玉米长期改良的目标性状,探索控制这些性状的有利等位基因的产生、在育种过程中的选择及其演化规律,也是今后重要的研究课题,并将为玉米育种提供理论指导和重要的遗传资源。

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