王夏青^,, 宋伟^,, 张如养, 陈怡凝, 孙轩, 赵久然^,北京市农林科学院玉米研究中心/玉米DNA指纹及分子育种北京市重点实验室,北京100097

Genetic Research Advances on Maize Stalk Lodging Resistance

WANG XiaQing^,, SONG Wei^,, ZHANG RuYang, CHEN YiNing, SUN Xuan, ZHAO JiuRan^,Maize Research Center, Beijing Academy of Agriculture & Forestry Sciences/Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Beijing 100097

通讯作者: 赵久然,E-mail：maizezhao@126.com

王夏青和宋伟为同等贡献作者。
责任编辑: 李莉
收稿日期:2020-07-23接受日期:2020-12-25网络出版日期:2021-06-01

基金资助:

北京****计划.BSP041 北京市农林科学院基因组学育种协同创新中心建设项目.KJCX201907-2 北京市农林科学院青年基金.QNJJ201931

Received:2020-07-23Accepted:2020-12-25Online:2021-06-01
作者简介 About authors
王夏青,E-mail：xiaqingwang427@163.com。

宋伟,E-mail：songwei1007@126.com。







摘要
茎秆倒伏严重影响玉米产量、品质和机械化收获,是当前玉米生产和育种亟待解决的主要问题之一。加强对玉米茎秆抗倒伏性的研究,对提高品种抗倒伏能力具有重要意义。本文综述了玉米茎秆倒伏的主要影响因素及其遗传特征。茎秆倒伏与茎秆自身的强度密切相关。茎秆强度越高,抗倒伏性越强。茎秆强度受茎秆所处的发育阶段、茎秆内部结构和外部形态,及其细胞壁成分等影响。处于分生组织的茎秆细胞分裂旺盛,较易折断,而进入生殖生长后,茎秆表皮、厚壁组织增厚,维管束发育成熟,对茎秆的支撑作用增强。茎秆细胞壁的主要成分——纤维素、半纤维素、木质素、可溶性糖、无机物等均可提升茎秆强度。目前,研究者借助高通量表型平台,利用玉米连锁群体和自交系群体,采用各种定位方法,鉴定到一系列影响茎秆形态、强度、细胞壁成分的相关QTL和候选基因。研究表明,基于单倍型的QTL定位方法比基于单个SNP的定位效果好。一致性QTL分析将不同遗传群体的研究整合到一起,能够提高QTL结果的通用性。茎秆强度的遗传基础复杂,受微效多基因控制,位点间具有加性效应。茎秆成分QTL中的候选基因涉及细胞壁代谢、转录因子、蛋白激酶等。MAIZEWALL是玉米细胞壁相关基因的重要数据库。目前该数据库包含1 156个玉米细胞壁生物学相关的候选基因,为该领域的深入研究提供强大的资源。已鉴定到一系列影响玉米茎秆细胞壁成分、茎秆形态和强度的基因,其功能涉及纤维素合成路径,如纤维素合成酶类、Cobra类、糖基转移酶和核糖转运蛋白类;苯丙烷路径基因,如控制bm1—bm5的相关基因;植物激素类,如赤霉素、生长素、油菜素甾醇相关基因;转录因子如NAC、MYB;miRNA（ZmmiR528）以及F-box基因（stiff1）等。今后应积极探索不同发育时期玉米茎秆倒伏的力学机制;广泛发展自然群体或育种群体进行遗传分析;采取多种定位策略,提高抗倒伏相关基因鉴定的功效;针对优良等位基因,开发各类分子标记,加强抗倒伏分子标记辅助选择。本文将为玉米茎秆抗倒伏遗传机制解析及抗倒伏玉米品种的分子育种提供参考。
关键词： 玉米;倒伏;茎秆;细胞壁;遗传研究

Abstract
Maize stalk lodging has a great adverse effect on yield, quality and mechanized harvesting, and is one of the main problems to be solved urgently in current maize production and breeding. Strengthening the research on the lodging resistance of maize stalk will have great significance for improving the lodging resistance of maize. In this paper, we summarize the main factors affecting maize stalk lodging resistance, and their genetic mechanisms. The stalk lodging resistance is closely related to the stalk strength. The greater the stalk strength, the stronger the lodging resistance. The stalk strength is affected by the developmental stage, the internal and external structures of the stalk, and the components of the stalk cell wall. The meristem zone has vigorously dividing cells and is easily broken. After entering the reproductive growth, the rind and sclerenchyma tissue of the stalk are thickened, the vascular bundles are mature, and thus the stalk strength is enhanced. The main components of the stalk cell wall, including cellulose, hemicellulose, lignin, soluble sugars, inorganic substances, can improve the strength of the stalk. To date, based on the high-throughput phenotyping platforms, various maize linkage and natural populations, and mapping methods, researchers have identified a series of QTLs and candidate genes that affect stalk morphology, strength, and cell wall components. The studies have shown that the haplotype-based mapping method is better than SNP-based mapping method. Meta-QTL analysis integrates the mapping results of different genetic populations and can improve the versatility of QTLs. The genetic basis of stalk strength is complex, which is determined by polygenes with minor effect and additive effect. Candidate genes in the QTLs involve cell wall metabolism, transcription factors, protein kinases, and so on. MAIZEWALL is an important database of genes related to maize cell wall. So far, the database contains 1 156 candidate genes related to maize cell wall biology, which provides a powerful resource for research in this field. A series of genes affecting cell wall components, stalk morphology and stalk strength in maize have been identified. Their functions of these genes are related to cellulose synthesis pathways, such as genes of cellulose synthase, Cobra, glycosyltransferase and ribose transport; phenylpropane pathway genes, such as genes regulating bm1-bm5; plant hormones genes, such as genes related to gibberellin, auxin and brassinosteroid; transcription factors such as NAC, MYB; miRNA (ZmmiR528) and F-box genes (stiff1). In the future research, it is needed to explore the mechanical mechanism of stalk lodging at different developmental stages. Develop diverse natural populations and breeding materials for genetic analysis. Employ a various of mapping strategies to improve the efficiency of identification of the QTL and genes related to lodging resistance. Design various molecular markers based on the favorable alleles to improve the molecular marker assisted selection for lodging resistance. These efforts will promote the research of the genetic mechanism of stalk lodging resistance, and provide a reference for the molecular breeding of new varieties with strong lodging resistance.
Keywords：maize;lodging;stalk;cell wall;genetic mechanism


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本文引用格式
王夏青, 宋伟, 张如养, 陈怡凝, 孙轩, 赵久然. 玉米茎秆抗倒伏遗传的研究进展[J]. 中国农业科学, 2021, 54(11): 2261-2272 doi:10.3864/j.issn.0578-1752.2021.11.002
WANG XiaQing, SONG Wei, ZHANG RuYang, CHEN YiNing, SUN Xuan, ZHAO JiuRan. Genetic Research Advances on Maize Stalk Lodging Resistance[J]. Scientia Acricultura Sinica, 2021, 54(11): 2261-2272 doi:10.3864/j.issn.0578-1752.2021.11.002


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近年来,中国玉米育种水平发展迅速,籽粒机械化直收进程加快,但不利气候因素持续增多,由此带来的倒伏问题对玉米生产的影响日益突出,成为限制玉米高产稳产和节本增效的主要问题之一^[1]。当前中国正处于从传统农业向现代化农业转型的关键时期,提高玉米品种茎秆抗倒伏性将会有效促进收获方式的变革,提高资源利用率和劳动生产力,降低生产成本和大面积减产的风险,增强中国玉米市场竞争力。

随着玉米遗传研究手段的快速发展,国内外****致力于利用基因组学、表型组学等多组学与传统遗传学相结合的手段,对茎秆发育、茎秆强度、形态及成分等影响玉米茎秆抗倒伏相关性状的生理、生化和遗传特性进行较为深入的研究,促进了茎秆抗倒相关基因的克隆及其功能解析。

1 茎秆倒伏的发生与危害

倒伏是植株茎秆从自然直立状态到永久错位的现象。倒伏破坏植物原有的空间分布,影响植株的光合叶面积及水分和养分运输;同时还会造成叶片、茎秆的损伤,促使病原菌和昆虫入侵,加剧病虫害发生,影响机械化作业,最终导致作物产量、品质和生产效率大幅降低^[2]。据统计,中国每年因倒伏造成玉米产量损失近100万t^[3]。玉米倒伏率每增加1%,减产约108 kg·hm^-2[4]。倒伏的发生主要受种植条件和品种特性影响。种植条件主要有风力和降雨等气候环境、种植密度和时间等种植方式、施肥量和生长调节剂等管理措施^[5];品种特性主要包括植株的根系结构、株型结构、茎秆特性等^[6,7]。

倒伏是一类较为复杂的性状,可发生在玉米生长的全生育期,包括苗期、拔节期、抽雄期、灌浆期、成熟期等。根据倒伏的部位,可分为根倒伏和茎倒伏。根倒伏是指植株不折断、不弯曲,从地表处连同根系一起倾斜歪倒（图1-A）。根倒伏容易在排水不良的土壤条件下发生,并且植株自身不能恢复直立生长^[8]。茎倒伏包括茎弯曲和茎折。茎弯曲是指茎秆弯曲和倾斜,一般发生在土壤紧实,且植株遭遇大风和降雨情况下（图1-B）。茎折是指植株从地上部某个节或节间处发生折断（图1-C）。据统计,玉米倒伏中30%—60%为茎倒伏,且茎折对产量的影响最大^[5,8]。抽雄前期发生茎折的部位大多在穗位节或穗上一节的基部^[9]（图1-C）。在玉米进入灌浆阶段,茎秆会把自身储存的有机物不断运往籽粒,可能会引起茎秆填充物减少,难以支撑果穗,促使穗下尤其是基部第3节茎折,造成产量损失,并影响玉米机械化收获^[1,2]（图1-D—图1-F）。

图1

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图1生产中常见的玉米倒伏类型

A：拔节期玉米根倒;B：抽雄前期茎弯曲和茎折;C：抽雄前期茎折;D：灌浆期的根茎复合倒伏;E：籽粒成熟后根倒伏和茎弯曲;F：籽粒成熟后茎秆基部第3节茎折
Fig. 1The common types of lodging in maize production

A: Root lodging in the jointing stage; B: The stalk bending and fracture in the early stage of tasseling; C: The stalk fracture in the early stage of tasseling; D: The compound lodging of the root and stalk after the grain filling stage; E: The root lodging and stalk bending after maturity; F: The fracture position was at the third internode after maturity

2 玉米茎秆抗倒伏的研究

2.1 茎秆抗倒伏的形态、生理及生化特征

茎秆在自然状态下的倒伏率是植株抗倒伏性的最直接表型,但该性状的影响因素较多,难以准确鉴定,因此,大部分研究用茎秆机械强度来评价植株的抗倒伏能力。茎秆机械强度反映茎秆的承受力,分为茎秆硬度和茎秆柔韧度。茎秆硬度可以通过茎皮穿刺强度、茎秆弯折强度、茎秆弯曲强度等指标来评价,这些指标数值越大表明茎秆硬度越高^{[10,11,12,13]}。茎秆的柔韧度可以通过茎秆弯折角度来评价。在相同的环境下,茎秆弯折角度越大,柔韧性越好,抗风性越好。相反,柔韧性较差的茎秆通常较脆,易出现茎折^[14]。茎秆强度受多方面因素影响,除了病虫害以外,更重要的是茎秆自身特性,包括茎秆所处的发育阶段、茎秆内部结构特征、茎秆长度、粗度及其细胞壁成分等。

茎秆的发育涉及诸多重要的生物学过程,如细胞分裂、细胞壁合成及维管束形成等。茎秆由节间和节点组成的多个重复单元构成,这些重复单元间存在较强的时空特异性^[15]。玉米任意一节茎秆均可以分为4个区域,即居间分生组织区、细胞伸长区、过渡区和成熟区^[9,16-17]。居间分生组织位于节间基部,具有较强的分裂能力,产生的大部分细胞最终发育成零散的维管束、内皮层、厚壁组织等^[18]。细胞伸长区靠近居间分生组织,该区域细胞不断膨大,初生细胞壁开始合成。过渡区位于伸长区之上,其细胞膨胀减慢并且次生细胞壁开始形成。成熟区位于每节茎秆的顶部位置,其细胞扩张停止^[15]。在不同生长时期,茎秆各发育区域的细胞壁成分存在较大差异。玉米抽雄前期,分生组织区的DNA和蛋白质合成旺盛,而纤维素、半纤维素、木质素和次生代谢物积累较少,导致该区域易折^[9]。当玉米进入生殖生长后,分生组织区的次生细胞壁开始积累,茎秆硬度明显提高,断裂的情况减少^[9]。

发育成熟的玉米茎秆解剖结构包括表皮、厚壁组织、维管束、薄壁组织等,其中,维管束又包括木质部和韧皮部。厚壁组织细胞均匀加厚且呈木质化,也称为机械组织,对茎秆的机械支撑尤为重要。研究表明茎秆厚壁组织比例、维管束鞘厚度、硬皮细胞腔隙厚度、维管束密度、维管束面积与茎秆强度显著正相关^[19,20]。此外,维管束的形状也会影响茎秆硬度和抗倒伏性^[21,22]。

节间长度和粗度是影响茎秆强度的重要形态因素。穗下节间较长、株高和穗位高较高,或者穗位高与株高比值较大等特征都增加了倒伏的风险^[23]。植株基部节间短且粗的品种通常抗倒伏性较好,尤其是基部第3节间的粗度与抗倒伏性呈极显著正相关^[4]。

茎秆化学组成指茎秆的细胞壁组分,主要包括纤维素、半纤维素、木质素、可溶性糖、无机物,以及量少但功能重要的膨胀素、果胶等^[24]。纤维素是植物细胞壁中最大的高分子聚合物,由β-1,4-葡萄糖残基通过较强的氢键连接而成^[25],是细胞壁中决定强度的主要物质。半纤维素是一类广泛的多糖,其主要功能是与纤维素和木质素相互作用以稳定细胞壁^[26]。木质素是植物细胞壁中仅次于纤维素的第二大高分子聚合物,主要在加厚的次生细胞壁中积累,是决定细胞壁强度和茎秆硬度的主要成分之一^[27]。茎秆中纤维素、半纤维素、木质素含量与茎秆强度正相关,某种或几种物质含量降低或此消彼长将引起茎秆变脆^[21,22]。此外,茎秆中的氮素含量、茎秆含水量及单位长度茎秆的重量也会影响倒伏。随施氮量增加,茎秆中淀粉、纤维素、木质素含量降低,茎秆倒伏率升高^[28]。茎秆的干物重与植株抗倒伏性呈显著正相关^[29]。

2.2 茎秆抗倒伏的QTL研究

目前,玉米茎秆强度的研究多集中于对茎秆硬度遗传位点的挖掘,而关于茎秆柔韧性的研究较少（表1）。茎秆强度的遗传力较低,需要在不同环境下检测,以最优线性无偏预测方法（best linear unbiased prediction,BLUP）来提高表型的准确性,基于BLUP数据得到的QTL结果优于单环境下的定位结果^[8,9,10]。茎皮穿刺强度比茎秆弯折强度的遗传力高,且该性状与茎秆强度和倒伏的相关性较高^[12]。茎秆强度的遗传基础复杂,受大量微效位点控制,各位点间存在加性效应,对茎秆强度的改良可以通过多个优良基因的聚合实现^[11,13]。目前,已经鉴定到控制玉米茎秆强度的基因stiff1^[30]。针对玉米茎秆柔韧性,WANG等^[14]鉴定到一个与茎秆弯折角度相关的QTL,并提出候选基因可能与RING/U box泛素蛋白和MADS转录因子相关。

Table 1
表1
表1玉米茎秆抗倒伏相关性状遗传定位统计
Table 1The summary of genetic studies for stalk lodging resistance traits in maize

序号 Order	性状 Trait	材料 Material	定位方法 Mapping method	主要结果 Main result	文献 Reference
1	茎秆弯曲强度 Stalk bending strength	216个RIL家系(B73×Ce03005) 216 RILs (B73×Ce03005)	复合区间作图 CIM	微效多基因遗传特征 Polygenic with minor effect inheritance	[10]
2	茎皮穿刺强度 Rind penetrometer strength	4692个NAM家系,及 196个IBM的RIL家系 4692 NAM, 196 IBM RILs	连锁分析、关联分析 Linkage analysis, GWAS	鉴定到与苯丙烷和纤维素合成相关的位点 QTLs were related to the synthesis of phenylpropane and cellulose	[11]
3	茎皮穿刺强度 Rind penetrometer strength	RIL家系(H127R× Chang7- 2)、(B73×By804) RILs (H127R× Chang7-2), (B73×By804)	复合区间作图 CIM	候选基因与细胞壁组分相关 Candidate genes were related to cell wall components	[12]
4	茎粗、茎秆弯曲强度、茎皮穿刺强度 Stalk diameter, stalk bending strength, rind penetrometer strength	257个自交系 257 inbred lines	多位点关联分析 Multi-locus association analysis	茎秆强度的改良可通过多个优良基因聚合实现 The improvement of stalk strength can be achieved through the accumulation of multiple favorable alleles	[13]
5	茎秆弯曲强度、茎皮穿刺强度 Stalk bending strength, rind penetrometer strength	189个RIL家系 (B73×Ki11) 189 RILs (B73×Ki11)	复合区间作图、关联 分析 CIM, GWAS	鉴定到一个控制茎秆强度的基因stiff1 stiff1 dominates stalk strength	[30]
6	茎秆柔韧度 Stalk flexibility	313个F2:3家系(J724×J724A1) 313 F2:3 (J724×J724A1)	混合群体分离分析 BSA	定位到1个控制茎秆柔韧度的QTL位点 One QTL was identified to control stalk flexibility	[14]
7	纤维素、半纤维、木质素 Cellulose, hemicellulose, lignin	368个自交系 368 inbred lines	关联分析 GWAS	候选基因涉及细胞壁代谢、转录因子、蛋白激酶 Candidate genes involve cell wall metabolism, transcription factors, protein kinases	[31]
8	酸性洗涤纤维、中性洗涤纤维 Acid detergent fiber, neutral detergent fiber	368个自交系 368 inbred lines	关联分析 GWAS	鉴定了ZmC3H2,提出56个候选基因 ZmC3H2 and 56 candidate genes were identified	[32]
9	6个细胞壁成分 6 cell wall components	188个RIL家系 (B73 ×By804) 188 RILs (B73×By804)	完备区间作图 ICIM	一半以上的QTL表型变异解释率超过10% More than half of the QTLs explained more than 10% phenotypic variation	[33]
10	木质素、葡萄糖和木糖 Lignin, glucose and xylose	263个IBM家系,以及 282个自交系 263 IBM, 282 inbred lines	连锁分析、关联分析 Linkage analysis, GWAS	鉴定到11个与木质素和含糖量有关的QTL 11 QTLs were related to lignin and sugar content	[34]
11	木质素及其单体含量 Lignin and its monomer content	242个RIL家系(F838×F286) 242 RILs (F838×F286)	复合区间作图 CIM	定位了80个QTL,包含7个热点区 80 QTLs were mapped, including 7 hot spots	[35]
12	细胞壁成分 Cell wall components	11个群体 11 populations	一致性QTL分析 Meta-QTL analysis	鉴定到与细胞壁组成、秸秆消化率相关的QTL QTLs related to cell wall composition and straw digestibility were identified	[36]
13	糖分含量 Stalk sugar content	202个RIL家系(YXD053×Y6-1) 202 RILs (YXD053×Y6-1)	复合区间作图 CIM	QTL之间有较强的上位性 QTLs with strong epistasis effect	[37]
14	株高与穗位高比例 Ratio of ear height to plant height	183个热带玉米自交系 183 tropical maize inbred lines	单倍型关联分析 Haplotype GWAS	单倍型关联分析更适用于倒伏性状的定位 Haplotype GWAS was more efficient for the mapping of lodging-related traits	[38]
15	茎粗 Stalk diameter	17个群体 17 populations	一致性QTL分析 Meta-QTL analysis	20个茎粗的Meta-QTLs 20 Meta-QTLs were related to stalk diameter	[39]
16	玉米最上节茎秆的维管束数目 Vascular bundle number at the uppermost internode of maize stalk	866个BC2S3,HIF材料 866 BC2S3, HIF	多QTL模型 Multiple QTL mapping	维管束数目受大量微效的QTL控制 Vascular bundle number was dominated by many small-effect QTLs	[40]
17	茎皮厚度、维管束数目、密度、茎粗 Rind thickness, vascular bundle number and density, stalk diameter	942个玉米自交系 942 inbred lines	关联分析 GWAS	鉴定到3个控制维管束密度的QTL位点 Three loci were associated with vascular bundle density	[41]
18	30个维管束性状 30 vascular traits	480个玉米自交系 480 inbred lines	多位点关联分析 Multi-locus association analysis	鉴定到84个维管束表型候选基因 84 candidate genes were related to vascular bundle phenotype	[42]

CIM：复合区间作图;GWAS：关联分析;混合群体分离分析;BSA：混合群体分离分析;ICIM：完备区间作图
CIM: Composite interval mapping; GWAS: Genome wide association study; BSA: Bulked segregant analysis; ICIM: Inclusive composite interval mapping

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在茎秆成分的遗传研究中,由于细胞壁成分检测费用较高,因此,一些研究利用近红外模型对这些性状的预测值进行定位,或者利用范式纤维素测定法对茎秆中的酸性洗涤纤维、中性洗涤纤维进行检测和定位^[31,32,33]（表1）。细胞壁成分相关QTL的候选基因涉及细胞壁代谢、转录因子、蛋白激酶等,并且一些QTL同时影响纤维素和木质素^[34]。BARRIèRE等^[35]在全基因组上鉴定到7个与木质素含量及其成分相关的QTL热点区域,分别位于Chr.1、Chr.3、Chr.8和Chr.10。TRUNTZLER等^[36]采用Meta-QTL方法,对11个作图群体的QTL进行整合,鉴定到大量与细胞壁组成、秸秆消化率相关的QTL。对茎秆中可溶性糖（白利度）研究表明,QTL之间具有较强的上位性,但QTL与环境的互作效应不强^[37]。

茎秆形态和解剖结构相关研究表明,基于单倍型的定位比基于单个SNP的定位效果更加理想,体现在QTL数目和QTL的表型变异解释率方面^[38]（表1）。刘福鹏等^[39]利用Meta-QTL分析方法,将17个不同作图群体的95个玉米茎粗QTL整合到IBM neighbors 2008高密度分子标记连锁图谱上,通过一致性分析方法得到20个一致性高的玉米茎粗QTL（Meta-QTL）。茎秆解剖结构特征的获取依赖于高精度的茎秆解剖结构图形,以及基于图形获得的各性状的量化值。HUANG等^[40]利用光学显微镜和图像处理软件获得866份大刍草和玉米BC₂S₃家系最上节茎秆维管束数目,定位结果表明该性状受大量微效QTL控制。MAZAHERI等^[41]利用扫描仪获得茎秆横切面照片,基于代码版的图像处理软件,获得942份玉米自交系的茎皮厚度、维管束密度、面积等表型,并检测到3个控制维管束密度的位点。近年来,X光-计算机断层扫描技术（X-ray microcomputed tomography,CT）的应用,极大地推进了对茎秆解剖特征的遗传研究。ZHANG等^[42]利用CT扫描获得玉米茎秆维管束的微观表型,并开发了一套基于茎秆横截面图像提取茎秆微观特征的流程,实现了对维管束数目、面积、大小等特征的统计。利用该技术对480份玉米自交系提取了30个茎秆解剖结构特征,并结合关联分析鉴定到大量涉及细胞壁代谢、转录因子、蛋白激酶相关的候选基因。

2.3 茎秆抗倒伏的候选基因研究

MAIZEWALL数据库是玉米细胞壁相关基因的重要数据库（http://www.polebio.scsv.ups-tlse.fr/MAIZEWALL/index.html）,存储了玉米与水稻和拟南芥细胞壁发育相关基因同源的EST序列^[43]。PENNING等^[44]在这些EST序列基础上,预测和注释了750个玉米细胞壁生物学相关基因（https://cellwall.genomics.purdue.edu/）。迄今为止,该数据库包含1 156个候选基因,为玉米细胞壁生物学的研究提供了强大的资源^[44]。其中,注释的纤维素相关基因包括33个CesA/Csl（cellulose synthase-like）超家族基因、9个Cobra类基因、38个核糖转化基因。半纤维素相关的基因有213个,包括49个GT8（glycosyl transferase8,糖基转移酶8）、54个GT47、19个GT37、18个GT34、41个GT31和32个木葡聚糖β-内转葡糖基酶/水解酶基因（xyloglucan endo-β-transglucosylase/hydrolase genes,XTH）。苯丙烷相关的基因共有102个。

目前,已鉴定到一些影响玉米茎秆细胞壁成分、茎秆形态和茎秆强度的基因,其功能涉及纤维素合成、苯丙烷路径、植物激素、转录因子、miRNA、F-box等（图2）。

图2

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图2茎秆抗倒伏遗传机制

Fig. 2The genetic mechanism of stalk lodging resistance



2.3.1 纤维素合成相关基因对茎秆抗倒伏的影响 纤维素是由几种不同的纤维素合酶（cellulose synthase,CesAs）复合物催化UDP-葡萄糖合成葡聚糖链,最终形成^[45]。影响纤维素含量的基因主要涉及：纤维素合成酶类基因、Cobra类基因、糖基转移酶和核糖转运蛋白基因等^[46,47,48]。研究发现,玉米脆秆突变体bk2为隐性突变体,其地上部分易折,且该表型只在第5片叶以后出现^[21]。Bk2编码COBRA蛋白,与水稻BC1和拟南芥COBRA- LIKE4同源。该基因的启动子及第二个外显子区域的转座子插入均可导致基因活性改变,纤维素总量下降40%,而非结构性碳水化合物含量则补偿性增加^[21]。

玉米中另一个茎秆突变体bk4在Mu突变体与自交系杂交的F₂群体中发现,茎秆较脆,易被强风折断,且株高降低,叶尖衰老以及花粉半不育^[22]。几丁质酶样蛋白（ZmCtl1）属于糖基水解酶,导致bk4茎秆变脆,该蛋白在延伸的节间中含量最高,并且ZmCtl1与纤维素合成酶基因CesA互作。该基因突变导致茎秆中对香豆酸、葡萄糖、甘露糖和纤维素含量显著降低,叶片和茎秆中细胞木质素染色减少、维管束变形、木质部和韧皮部受损。CTL1蛋白在植物中有较高的保守性,为不同作物抗倒伏品种培育提供了新的途径。

2.3.2 苯丙烷类基因对茎秆抗倒伏的影响 木质素的生物合成起始于苯丙烷途径,该途径产生多种木质素前体,包括香豆醇、松柏醇和芥子醇^[49]。目前,已鉴定到5个影响玉米木质素组分含量及茎秆强度的棕色叶脉突变体bm1—bm5及其相关基因。

bm1编码肉桂醇脱氢酶（cinnamyl alcohol dehydrogenase,CAD）^[50]。bm1突变体的特征比较单一,在木质化组织中,其CAD活性严重降低,导致木质素的总量和木质素单体的结构均发生改变^[50]。

bm2编码亚甲基4氢叶酸还原酶（methylenetetrahydrofolate reductase,MTHFR）^[51]。MTHFR生成5-甲基四氢叶酸,用于半胱氨酸的甲基化以生成甲硫氨酸。随后,通过S-腺苷甲硫氨酸合成酶的作用从甲硫氨酸产生S-腺苷-L-甲硫氨酸（S-adenosyl-_L- methionine,SAM）,而SAM是咖啡酰辅酶A 3-O-甲基转移酶（caffeoyl CoA 3-O-methyltransferase,CCoAOMT）和咖啡酸-O-甲基转移酶（caffeic acid 3-O-methyltransferase,COMT）的甲基供体。因此,MTHFR功能的改变会影响SAM的积累,进而减少S型和G型木质素的积累以及总木质素水平^[51]。

bm3编码咖啡酸-O-甲基转移酶（COMT）^[52]。bm3的等位基因突变体都是由于反转录转座子插入造成mRNA水平下降引起。

bm4编码叶酰聚谷氨酸合酶（folylpolyglutamate synthase,FPGS）,该酶在单碳代谢中成为叶酸依赖性酶的聚谷氨酸底物^[53]。相对于野生型,bm4突变体的木质素浓度适度降低,而S﹕G木质素比例总体增加。

bm5编码4-香豆酸-辅酶A连接酶1（4-coumarate: CoA ligase 1,4CL1）,该酶可将对香豆酸酯、咖啡酸酯和阿魏酸酯转化为其相应的CoA酯^[54]。bm5突变体成熟茎中Klason木质素、G型木质素和对香豆酸盐的水平降低,但H型木质素和阿魏酸盐的水平增加,导致其茎秆和叶片中脉呈棕褐色。Zm4CL1存在2个独立的突变,其中第一个外显子插入了658 bp的Ac转座子,导致氨基酸编码提前终止,4CL1酶活力丧失;而第二个内含子中插入的283 bp转座子,导致该内含子被剪切,使基因表达量降低。这两种变异均使G型木质素生物合成减少,而可溶性阿魏酸衍生物含量增加,但总木质素含量没有发生变化^[54]。

2.3.3 植物激素对茎秆抗倒伏的影响 玉米中鉴定到较多影响节间长度的突变体,这些突变体同时还影响了株高和抗倒伏性。相关基因主要涉及植物激素类,包括赤霉素（Gibberellin,GA）、生长素（Auxin,IAA）、油菜素甾醇（Brassinosteroid,BR）等。

赤霉素是异戊二烯植物激素,是高等植物茎伸长必需的激素。赤霉素相关突变体中影响节间长度的有an1、dwarf3、dwarf8等^[55,56,57]。An1催化贝壳杉烯合成,是赤霉素生物合成途径的早期基因,该基因的突变体整体节间缩短、株高降低、发育迟缓^[55]。Dwarf3（D3）是编码细胞色素P450家族的基因^[56]。dwarf8突变体是显性突变,由GA抑制剂DELLA蛋白的VHYNP结构域中单个氨基酸插入造成基因功能改变,使得节间缩短、株高降低^[57]。

影响节间长度的油菜素甾醇突变体包括na1、brd1、dwf1和dwf4等^[58,59]。nana plant1（na1）由于油菜素甾醇合成路径中DET2蛋白功能缺失造成穗下节间极度缩短、植株矮小^[58]。Brd1编码油菜素甾醇C-6氧化酶,该基因的突变体在播种10 d以后节间几乎不伸长,植株极端矮化^[59]。

涉及生长素合成和转运相关路径的基因突变也影响节间长度,包括吲哚3-乙酰胺（Indole 3-acetamide,IAM）、吲哚3-丙酮酸（Indole 3-pyruvate,IPA）、色胺（Tryptamine,TAM）途径,以及输入载体AUX/LAX和输出载体PIN、PGP等。典型的生长素相关节间突变体为br2、bv1^[60,61]。Br2参与生长素极性运输,可显著降低穗位下方的节间长度,造成株高降低50%以上^[60]。小株突变体（bv1）基因编码多磷酸肌醇-5-磷酸酶,突变后节间细胞长度变短,致使节间缩短,株高降低^[61]。此外,植物激素还对茎粗有影响,例如,Br2在降低节间长度的同时使茎粗增加^[60,62]。

2.3.4 转录因子对茎秆抗倒伏的影响 在模式植物拟南芥和其他作物中,已经鉴定出NAC、MYB等一系列影响次级细胞壁发育的重要转录因子^[63]。典型的转录因子包括NAC次生壁加厚促进因子1（NAC secondary wall thickening promoting factor 1,NST1）、NST2、NST3、维管束相关的NAC结构域（vascular- related NAC-domain,VND1-7）^[64],R2R3-MYB家族等^[65]。此外,NAC转录因子能够调控较多影响细胞壁成分相关的转录因子,如调控SND2、SND3、MYB20、MYB42、MYB43、MYB52、MYB54、MYB69、MYB85、MYB103、KNYT7等^[63,66]。在玉米中鉴定到NAC转录因子基因ZmNST3和ZmNST4参与次级细胞壁的发育,超表达后次级细胞壁积累较多,并且这两个基因可以调控纤维素相关基因ZmMYB109、ZmMYB128、ZmMYB149的表达,暗示ZmNST3和ZmNST4是玉米次级细胞壁生物合成过程的主要开关^[67]。

2.3.5 miRNA对茎秆抗倒伏的影响 植物体内的miRNA表达水平会随着氮素含量的变化而改变。ZmmiR528是单子叶特异的miRNA,在茎秆维管束中表达。玉米在高氮条件下,体内的ZmmiR528表达量升高,而编码木质素合成相关的漆酶基因ZmLAC3和ZmLAC5是ZmmiR528的靶标,因此导致木质素3个单体及总量的合成减少、茎皮穿刺强度降低、茎秆抗倒伏性下降。相反,敲除ZmmiR528后,木质素总量升高,茎秆抗倒伏性提高^[68]。

2.3.6 F-box蛋白对茎秆抗倒伏的影响 F-box是植物界中最大的蛋白质家族之一,在植物胁迫、激素信号传导、生长发育和miRNA生物过程中均起作用^[69]。ZHANG等^[30]调查了B73×Ki11的RIL群体茎秆弯折强度和茎皮穿刺强度,结合茎秆中的表达量差异,定位到编码F-box结构域的stiff1（Zm00001d036653）。该基因的功能位点是启动子区域27.2 kb的Ty1/Copia类转座子插入,抑制stiff1的表达,促进了GA和IAA的上调,进而激活与次级细胞壁发育相关的NAC、MYB转录因子,促进细胞壁中纤维素和木质素含量增加、茎秆厚壁细胞增厚,茎秆强度提高。利用CRISPR/Cas9基因编辑技术敲除stiff1后,玉米茎秆强度及抗倒伏性增强。进化分析发现,以B73为代表的大部分玉米坚秆材料都含stiff1的优良等位基因,这些材料在启动子区域受到较强的选择,表明该基因在坚秆材料的改良和育种中起到重要作用^[30]。

3 展望

茎秆抗倒伏是较为复杂的性状,不同时期倒伏的类型和发生机制存在差异,应积极探索不同发育时期玉米的自然受风情况,对其力学机制进行深入研究,并分析茎秆的遗传、生理、生化等特征,明确影响阶段性倒伏差异的主要性状,并对其开展遗传研究。

茎秆抗倒伏相关表型获取的准确性是影响遗传定位的关键因素。高通量表型鉴定技术为大规模精准地调查群体的表型提供了可能^[41,42]。对不同时期茎秆抗倒伏的表型应不断细化,从宏观和微观角度加强对茎秆相关表型的获取。

茎秆倒伏相关性状呈现数量性状特征,随着不同遗传定位群体的兴起和统计模型的发展,对其遗传定位、优良等位基因挖掘成为可能。研究群体可充分利用变异广泛、定位功效高的群体,例如包含不同种质类型的关联群体、多亲本群体如巢式关联群体（nested association mapping,NAM）、多亲本高世代互交群体（multi-parent advanced generation intercross,MAGIC）、双列杂交与育种偏好性选择相结合的互交群体（complete-diallel design plus unbalanced breeding-like inter-cross,CUBIC）,以及精细定位群体如近等基因系（near isogenic line,NIL）、剩余杂合群体（heterogeneous inbred family,HIF）等^[70,71]。QTL检测模型多种多样,例如当前在关联分析中广泛应用的混合线性模型、多位点关联分析模型,双亲群体中的BSA、CIM、ICIM、GCIM等模型,基于单个SNP和单倍型的模型等^[72,73]。不同方法各具优势,可根据群体类型针对性地采取多方法互补定位策略,提高QTL的检测率和准确性。除了传统的基因克隆策略,还可以充分借鉴各物种中鉴定到的同源基因。候选基因结合使用高效的CRISPR/Cas9技术或者Mu和EMS突变体库,将加快对玉米茎秆抗倒伏相关基因的鉴定^[74,75]。

目前,玉米中鉴定到一些与茎秆抗倒伏相关的基因,但很少被广泛应用到分子标记辅助选择,其中一个重要因素是这些基因大多基于突变体克隆,因此,有必要利用自交系群体或育种材料,加强对抗倒伏相关基因的鉴定,筛选优良的等位基因。另一方面,玉米基因组中存在广泛的遗传连锁累赘和一因多效现象,操作一个基因的同时可能产生一些不利的表型;反之,也有可能对多个性状都有利。例如转录因子基因ZmNST3在增加茎秆维管束数目的同时,也可提高茎秆中纤维素、木质素的含量,同时还能增加植株的抗旱性能^[45,76]。对于这样的基因可以进一步深入研究和利用。最近鉴定到的茎秆强度相关基因stiff1是玉米中自然存在的有利变异,可以加强对该基因分子标记的应用,以提升玉米种质资源的茎秆强度^[30]。茎秆强度的改良还可通过聚合多个优良等位基因获得^[13]。因此,可以将影响茎秆强度不同性状或同一性状不同位点的优良等位基因聚合,开展茎秆强度的分子聚合育种,提高玉米抗倒伏分子育种效率。

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