玉米ZmICE2基因调控气孔发育

doi:10.11983/CBB22261

植物学报 ›› 2023, Vol. 58 ›› Issue (6): 866-881.DOI: 10.11983/CBB22261

玉米ZmICE2基因调控气孔发育

周文期¹^,^*(), 周玉乾¹, 李永生¹, 何海军¹, 杨彦忠¹, 王晓娟¹, 连晓荣¹, 刘忠祥¹, 胡筑兵²^,^*()

¹甘肃省农业科学院作物研究所, 兰州 730070
²河南大学生命科学学院, 省部共建作物逆境适应与改良国家重点实验室, 开封 475004

收稿日期:2022-11-14 接受日期:2023-04-18 出版日期:2023-11-01 发布日期:2023-11-27
通讯作者: * E-mail: zhouwenqi850202@163.com;zhubinghu@henu.edu.cn
基金资助:
河南大学省部共建作物逆境适应与改良国家重点实验室开放课题(2021KF04);兰州大学细胞活动与逆境适应教育部重点实验室开放基金(lzujbky-2022-kb03);国家自然科学基金(32160490);国家自然科学基金(31860384);甘肃省重大专项计划(21ZD11NA005);甘肃省重大专项计划(21ZD10NF003)

ZmICE2 Regulates Stomatal Development in Maize

Wenqi Zhou¹^,^*(), Yuqian Zhou¹, Yongsheng Li¹, Haijun He¹, Yanzhong Yang¹, Xiaojuan Wang¹, Xiaorong Lian¹, Zhongxiang Liu¹, Zhubing Hu²^,^*()

¹Crops Research Institute, Gansu Academy of Agricultural Sciences, Lanzhou 730070, China
²State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng 475004, China

Received:2022-11-14 Accepted:2023-04-18 Online:2023-11-01 Published:2023-11-27
Contact: * E-mail: zhouwenqi850202@163.com;zhubinghu@henu.edu.cn

摘要/Abstract

摘要： 植物表皮在调节光合作用、呼吸作用、热量散失和水分利用等方面发挥重要作用。在拟南芥(Arabidopsis thaliana)等双子叶植物中, 气孔发育机理研究取得显著进展, 报道了3个非常重要的bHLH正调控转录因子(SPCH、MUTE和FAMA), 它们在气孔系细胞分裂与分化的不同阶段特异表达, 分别与转录因子SCRM/ICE1和SCRM2/ICE2形成异二聚体, 共同调控气孔细胞系在3个分裂阶段的细胞形态转换和变化, 最终发育形成气孔复合体。然而, 在单子叶植物尤其是禾本科植物玉米(Zea mays)中, 调控表皮形态建成的基因研究较少。该文利用反向遗传学手段分离到2个单基因隐性遗传突变体Zmice1-1 (inducer of cbf expression1-1)和Zmice2-1, 与对照B73相比, Zmice2-1植株矮小, 叶片黄化, 育性降低, 叶片气孔密度和气孔指数极显著降低, 打破了1个气孔间隔1个表皮长细胞的排列模式; Zmice1-1从五叶一心期开始叶片逐渐发黄, 后期全部黄化, 生长停滞, 纯合不育, 其叶片气孔密度与对照无显著差异。利用CRISPR-Cas9基因编辑技术获得不同位点的等位突变体, 表型鉴定发现Zmice2-2具有气孔异常表型, 并且与Zmice2-1的气孔表型类似, 表明ZmICE2参与调控气孔发育。B73和Zmice2-1的转录组分析表明, ZmICE2主要通过影响细胞分裂和分化来调控气孔发育, 参与玉米表皮形态建成。研究结果有助于进一步完善玉米表皮形态建成机制, 并为提高农作物的抗逆性和产量性状的遗传改良提供了有益的基因资源。

关键词: 玉米, 气孔发育, 气孔密度, 表皮形态建成, CRISPR-Cas9基因编辑

Abstract: Plant epidermis is crucial in regulating photosynthesis, respiration, heat dissipation, and water utilization. Significant progress has been made in the study of stomatal development in dicotyledonous plants, such as Arabidopsis thaliana. Three important bHLH transcription factors (SPCH, MUTE, and FAMA) have been reported to be specifically expressed at different stages of cell division and differentiation in the stomatal lineage. They form heterodimers with another transcription factors SCRM/ICE1 and SCRM2/ICE2 to regulate the morphological transformation and changes of stomatal lineage cells across three stages of division, finally forming the stomatal complex. However, in monocots, especially in Poaceae plants such as maize (Zea mays), studies on genes regulating epidermal morphogenesis are less reported. In this study, two single-gene recessive mutants, Zmice1-1 (inducer of cbf expression1-1) and Zmice2-1, were isolated using reverse genetics approaches. Compared to the control B73, Zmice2-1 exhibited dwarfism, leaf chlorosis, reduced fertility, significantly lower stomatal density and index, disrupted arrangement of epidermal long cells, and absence of spacing between stomata. Zmice1-1 leaves gradually turned yellow from the five-leaf stage and displayed complete chlorosis at later stages. The homozygous Zmice1-1 plants are growth-arrested and sterile, but the stomatal density showed no significant difference compared to the control. Different allels of Zmice2 were obtained using CRISPR-Cas9 genome editing technology. Phenotypic identification showed that Zmice2-2 had an abnormal stomatal phenotype similar to Zmice2-1, indicating that ZmICE2 is involved in the regulation of stomatal development. Transcriptome analysis of B73 and Zmice2-1 revealed that ZmICE2 primarily regulated stomatal development by affecting cell division and differentiation, participating in the formation of maize epidermal morphology. These results contribute to a better understanding of the mechanisms of epidermal morphogenesis in maize and provide valuable genetic resources for improving crop resilience and yield traits.

Key words: maize, stomatal development, stomatal density, epidermal morphogenesis, CRISPR-Cas9 gene editing

周文期, 周玉乾, 李永生, 何海军, 杨彦忠, 王晓娟, 连晓荣, 刘忠祥, 胡筑兵. 玉米ZmICE2基因调控气孔发育. 植物学报, 2023, 58(6): 866-881.

Wenqi Zhou, Yuqian Zhou, Yongsheng Li, Haijun He, Yanzhong Yang, Xiaojuan Wang, Xiaorong Lian, Zhongxiang Liu, Zhubing Hu. ZmICE2 Regulates Stomatal Development in Maize. Chinese Bulletin of Botany, 2023, 58(6): 866-881.

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链接本文: https://www.chinbullbotany.com/CN/10.11983/CBB22261

https://www.chinbullbotany.com/CN/Y2023/V58/I6/866

图/表 9

表1 本研究使用的引物序列

Table 1 Primer sequences used in this study

Primer name	Forward primer (5′-3′)	Reverse primer (5′-3′)
ZmICE2	ACCCCAACAAAACCAGGAC	GTCTCTTTTTCAGCGGTCTTG
T-ice2-1	GAGGAGGACGACGACAAGAAG	GCTAATTGCTACCGAAAACGC
T-ice1-1	GCGACCCATCAACCCATAGC	CGGTGTTGATGGGTTGAAGC
T-ice2-c9	ACGAGAATGGGTGAGTGTGG	AAGAGCGAGAACATCTGCGA
GAPDH	CCATCACTGCCACACAGAAAAC	AGGAACACGGAAGGACATACCAG
RT-ZmICE2	CTTCCTCGGGCGGCGGCGGTG	ACCGTGCTGTTGGCGTTGGAG

图1 Zmice1-1和Zmice2-1突变体苗期田间表型 (A)-(C) Zmice2-1突变体, 苗期表现出黄叶表型, 且株型矮小; (D), (E) Zmice1-1突变体, 五叶一心期开始出现黄化性状, 后期表型更加明显; (F), (G) Zmice2-1和Zmice1-1株高和穗位高度比对照极显著降低(**表示差异极显著(P<0.01))。(G)图中由于Zmice1-1纯合体一直未能发育出雌穗, 因此统计穗位为成熟期倒6叶距离地面的高度。(B), (C), (D) Bars=10 cm; (A), (E) Bars=20 cm

Figure 1 Field phenotypes of Zmice1-1 and Zmice2-1 mutants at seedling stage (A)-(C) Zmice2-1 mutant showed yellow leaf phenotype and short plant type at seedling stage; (D), (E) From the five-leaf and one-heart stage, the Zmice1-1 leaves gradually began to turn yellow, and the phenotype became more obvious at the later stage; (F), (G) The plant height and ear height of Zmice2-1 and Zmice1-1 were significantly decreased compared with the control (** indicate extremely significant differences (P<0.01)). In the figure (G), since the homozygote of Zmice1-1 had not developed a female spike, the spike height was calculated as the height from the ground of the fallen 6 leaves at maturity stage. (B), (C), (D) Bars=10 cm; (A), (E) Bars=20 cm

图2 Zmice1-1和Zmice2-1突变体气孔分布图式 (A) B73幼苗叶片气孔及表皮细胞图式(1个气孔间隔1个表皮长细胞, 呈单线性规则排列); (B) Zmice2-1幼叶气孔及表皮细胞图式(相同大小视野中气孔密度显著降低); (C) Zmice1-1幼叶气孔及表皮细胞图式(与对照无显著差异); (D) B73表皮细胞形态; (E) Zmice2-1结实期表皮细胞形态(气孔数目少); (F) Zmice1-1结实期叶片气孔及表皮扁平细胞形态(气孔开度增加)。箭头指示未发育成成熟气孔。Bars=20 μm

Figure 2 Morphology and stomatal distribution of Zmice1-1 and Zmice2-1 mutants (A) Schematic diagram of stomata and epidermal cells in leaves of B73 seedlings (with one stomata spaced by one epidermal long cell in a monolinear regular arrangement); (B) Stomata and epidermal cell schema of young leaves of Zmice2-1 (there were only a few stomata in the same size field of vision, and stomatal density decreased significantly); (C) Stomata and epidermal cell pattern of Zmice1-1 young leaves (showed no significant difference from the control); (D) Epidermal cell morphology of B73; (E) The epidermal cell morphology of Zmice2-1 (in the setting stage number of stomata reduced); (F) Stomatal morphology and epidermal flat cell morphology of leaves at Zmice1-1 setting stage (with increased stomatal opening). Arrows indicate immature stomatas. Bars=20 μm

图3 B73和Zmice突变体气孔密度及气孔指数 (A), (B) 统计第3、4叶和第12、13叶气孔密度, Zmice2-1气孔密度较对照极显著降低, Zmice1-1气孔密度无显著变化(n=200); (C), (D) 统计第3、4叶和第12、13叶气孔指数, Zmice2-1气孔指数较对照极显著降低, Zmice1-1气孔指数无显著变化(n=200)。n=200表示统计的气孔数目(≥15个显微视野), 3次生物学重复。** P<0.01

Figure 3 Stomatal density and stomatal index of B73 and Zmice mutants (A), (B) The stomatal density of the 3rd, 4th, 12th and 13th leaves was calculated, the stomatal density of Zmice2-1 was significantly lower than that of the control, while the stomatal density of Zmice1-1 showed no significant change (n=200); (C), (D) The stomatal indexes of the 3rd, 4th, 12th and 13th leaves were counted, Zmice2-1 stomatal indexes were significantly lower than that of the control, while Zmice1-1 stomatal indexes had no significant change (n=200). n=200 represented the statistical number of stomata (≥15 microscopic fields) and 3 biological replicates. ** P<0.01

表2 ZmICE2在不同物种中的基因编号及功能注释

Table 2 Gene code and function annotation of ZmICE2 in different species

Species	Homologous gene	The function of prediction
Arabidopsis thaliana	AT3G26744	Basic helix-loop-helix (bHLH) DNA-binding superfamily protein
Oryza sativa	LOC_Os11g32100	Inducer of CBF expression 1, putative, expressed
Brachypodium distachyum	Bradi4g17460	ICE87
Zea mays	GRMZM2G033356	Helix-loop-helix DNA-binding domain containing protein
Sorghum bicolor	Sb05g019530	Helix-loop-helix DNA-binding domain containing protein
Vitis vinifera	GSVIVG00008637001	Helix-loop-helix DNA-binding domain containing protein
V. vinifera	GSVIVG00032998001	Inducer of CBF expression 1
Populus trichocarpa	POPTR_0012s10780	ICE1; DNA binding/transcription activator/transcription factor
P. trichocarpa	POPTR_0015s11650	ICE1; DNA binding/transcription activator/transcription factor

图4 ZmICE2同源蛋白氨基酸序列比对及系统进化分析 (A) ZmICE2蛋白序列保守性分析(黑色表示氨基酸序列100%相同; 深灰色表示75%相同; 浅灰色表示50%相同); (B) ZmICE2蛋白同源树分析; (C) ZmICE2蛋白系统进化树分析

Figure 4 Sequence alignment of amino acid sequence of ZmICE2 with its homologues and phylogenetic analysis (A) Conservative analysis of ZmICE2 protein sequences (with black indicating 100% identical amino acid sequences; dark gray means 75% the same amino acid sequences; light gray means 50% the same amino acid sequences); (B) Homologous tree analysis of ZmICE2 protein; (C) Phylogenetic tree analysis of ZmICE2 protein

图5 B73与Zmice2-1差异表达基因的聚类分析 (A) 样品基于差异表达基因的相关性分析; (B) 差异表达基因的MA图(图中每个点表示1个基因); (C) 差异表达基因的聚类分析图(每行代表1个基因, 每列代表1个样品); (D) 转录本表达的箱线图(Zmice2-1中ZmICE2表达量降低)

Figure 5 Cluster analysis of differentially expressed genes in B73 and Zmice2-1 (A) Sample correlation analysis based on differential expression gene; (B) MA map of differentially expressed genes (each dot represents a gene); (C) Cluster analysis diagram of differentially expressed genes (each row represents a gene and each column represents a sample); (D) Boxplot of transcript expression (ZmICE2 expression decreased in Zmice2-1).

图6 B73与Zmice2-1差异表达基因的GO聚类

Figure 6 GO cluster of differentially expressed genes in B73 and Zmice2-1

图7 ZmICE2基因编辑突变体表型 (A) ZmICE2转基因试管苗; (B), (C) ZmICE2基因编辑T0代转基因田间植株表型; (D) T2代转基因田间植株表型(叶片黄化); (E), (F) 对照(CK)与Zmice2-2表皮气孔图式(Zmice2-2大量气孔缺失, 不能形成正常气孔)。箭头指示未发育成成熟气孔。(A)-(D) Bars=10 cm; (E), (F) Bars=20 μm

Figure 7 Phenotype of ZmICE2 gene editing mutant (A) ZmICE2 transgenic test-tube seedlings; (B), (C) Phenotype of ZmICE2 gene editing T0 generation transgenic plant in field; (D) Phenotype of T2 generation transgenic plant in field (leaf yellowing); (E), (F) The epidermal stomatal schema of control (CK) and Zmice2-2 (Zmice2-2 lacked a large number of stomata and could not form normal stomata). Arrows indicate immature stomata. (A)-(D) Bars=10 cm; (E), (F) Bars=20 μm

参考文献 57

[1]	陈亮, 侯岁稳 (2017). 植物气孔发育的分子遗传调控. 中国科学: 生命科学 47, 798-807.
[2]	陈青云 (2017). 玉米中STOMAGEN-Like基因调控气孔发育的功能研究. 硕士论文. 南宁: 广西大学. pp. 35-60.
[3]	刘延波, 项阳, 秦利军, 赵德刚 (2014). 转玉米ZmSDD1基因烟草降低气孔密度提高抗旱性. 植物生理学报 50, 1889-1898.
[4]	牛艳丽, 柏胜龙, 王麒云, 刘凌云 (2017). 单细胞组学技术及其在植物保卫细胞研究中的应用. 植物学报 52, 788-796. DOI
[5]	商业绯, 李明, 丁博, 牛浩, 杨振宁, 陈小强, 曹高燚, 谢晓东 (2017). 生长素调控植物气孔发育的研究进展. 植物学报 52, 235-240. DOI
[6]	王宏亮, 郭思义, 王棚涛, 宋纯鹏 (2018). 植物气孔发育机制研究进展. 植物学报 53, 164-174. DOI
[7]	张一弓, 张怡, 张怡, 阿依白合热木·木台力甫, 张道远 (2021). 异源过表达齿肋赤藓ScABI3基因改变拟南芥气孔表型并提高抗旱性. 植物学报 56, 414-421.
[8]	周文期 (2015). 调控水稻叶表皮发育的LPL2和DSP1基因克隆与功能分析. 博士论文. 兰州: 兰州大学. pp. 38-66.
[9]	周文期, 寇思荣, 连晓荣, 杨彦忠, 刘忠祥, 王晓娟, 何海军, 周玉乾 (2020a). 水稻和玉米叶表皮突变体的筛选和鉴定. 植物生理学报 56, 189-199.
[10]	周文期, 连晓荣, 周玉乾, 王兴荣, 杨彦忠, 刘忠祥, 王晓娟, 何海军, 寇思荣 (2020b). EMS诱变玉米自交系种质创新应用. 玉米科学 28(6), 31-38.
[11]	周玉乾, 孟思远, 周文期 (2018). 植物表皮形态建成的分子调控机制. 西北农学报 27, 609-616.
[12]	周文期, 强晓霞, 王森, 江静雯, 卫万荣 (2022). 水稻OsLPL2/PIR基因抗旱耐盐机制研究. 作物学报 48, 1401-1415. DOI
[13]	周玉萍, 颜嘉豪, 田长恩 (2022). 保卫细胞中ABA信号调控机制研究进展. 植物学报 57, 684-696. DOI
[14]	Bergmann DC, Sack FD (2007). Stomatal development. Annu Rev Plant Biol 58, 163-181. PMID
[15]	Caine RS, Yin XJ, Sloan J, Harrison EL, Mohammed U, Fulton T, Biswal AK, Dionora J, Chater CC, Coe RA, Bandyopadhyay A, Murchie EH, Swarup R, Quick WP, Gray JE (2019). Rice with reduced stomatal density conserves water and has improved drought tolerance under future climate conditions. New Phytol 221, 371-384. DOI PMID
[16]	Chater CCC, Caine RS, Fleming AJ, Gray JE (2017). Origins and evolution of stomatal development. Plant Physiol 174, 624-638. DOI PMID
[17]	Chen ZH, Chen G, Dai F, Wang YZ, Hills A, Ruan YL, Zhang GP, Franks PJ, Nevo E, Blatt MR (2017). Molecular evolution of grass stomata. Trends Plant Sci 22, 124-139. DOI URL
[18]	Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong XH, Agarwal M, Zhu JK (2003). ICE1: a regulator of cold- induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17, 1043-1054. DOI URL
[19]	Cuming AC, Cho SH, Kamisugi Y, Graham H, Quatrano RS (2007). Microarray analysis of transcriptional responses to abscisic acid and osmotic, salt, and drought stress in the moss, Physcomitrella patens. New Phytol 176, 275-287.
[20]	Deng CY, Ye HY, Fan M, Pu TL, Yan JB (2017). The rice transcription factors OsICE confer enhanced cold tolerance in transgenic Arabidopsis. Plant Signal Behav 12, e1316442. DOI URL
[21]	Dong CH, Agarwal M, Zhang YY, Xie Q, Zhu JK (2006). The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1. Proc Natl Acad Sci USA 103, 8281-8286. DOI URL
[22]	Edwards D, Kerp H, Hass H (1998). Stomata in early land plants: an anatomical and ecophysiological approach. J Exp Bot 49, 255-278. DOI URL
[23]	Feng F, Qi WW, Lv YD, Yan SM, Xu LM, Yang WY, Yuan Y, Chen YH, Zhao H, Song RT (2018). OPAQUE11 is a central hub of the regulatory network for maize endosperm development and nutrient metabolism. Plant Cell 30, 375-396. DOI URL
[24]	Frank MJ, Smith LG (2002). A small, novel protein highly conserved in plants and animals promotes the polarized growth and division of maize leaf epidermal cells. Curr Biol 12, 849-853. PMID
[25]	Gao Y, Wu MQ, Zhang MJ, Jiang W, Ren XY, Liang EX, Zhang DP, Zhang CQ, Xiao N, Li Y, Dai Y, Chen JM (2018). A maize phytochrome-interacting factors protein ZmPIF1 enhances drought tolerance by inducing stomatal closure and improves grain yield in Oryza sativa. Plant Biotechnol J 16, 1375-1387. DOI URL
[26]	Han SK, Qi XY, Sugihara K, Dang JH, Endo TA, Miller KL, Kim ED, Miura T, Torii KU (2018). MUTE directly orchestrates cell-state switch and the single symmetric division to create stomata. Dev Cell 45, 303-315. DOI URL
[27]	Han SK, Torii KU (2019). Linking cell cycle to stomatal differentiation. Curr Opin Plant Biol 51, 66-73. DOI URL
[28]	Hepworth C, Caine RS, Harrison EL, Sloan J, Gray JE (2018). Stomatal development: focusing on the grasses. Curr Opin Plant Biol 41, 1-7. DOI PMID
[29]	Jiang HF, Shi YT, Liu JY, Li Z, Fu DY, Wu SF, Li MZ, Yang ZJ, Shi YL, Lai JS, Yang XH, Gong ZZ, Hua J, Yang SH (2022). Natural polymorphism of ZmICE1 contributes to amino acid metabolism that impacts cold tolerance in maize. Nat Plants 8, 1176-1190. DOI PMID
[30]	Kanaoka MM, Pillitteri LJ, Fujii H, Yoshida Y, Bogenschutz NL, Takabayashi J, Zhu JK, Torii KU (2008). SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to Arabidopsis stomatal differentiation. Plant Cell 20, 1775-1785. DOI URL
[31]	Kidokoro S, Kim JS, Ishikawa T, Suzuki T, Shinozaki K, Yamaguchi-Shinozaki K (2020). DREB1A/CBF3 is repressed by transgene-induced DNA methylation in the Arabidopsis ice1-1 mutant. Plant Cell 32, 1035-1048. DOI URL
[32]	Lau OS, Bergmann DC (2012). Stomatal development: a plant’s perspective on cell polarity, cell fate transitions and intercellular communication. Development 139, 3683-3692. DOI URL
[33]	Li XM, Han HP, Chen M, Yang W, Liu L, Li N, Ding XH, Chu ZH (2017). Overexpression of OsDT11, which encodes a novel cysteine-rich peptide, enhances drought tolerance and increases ABA concentration in rice. Plant Mol Biol 93, 21-34. DOI URL
[34]	Liu T, Ohashi-Ito K, Bergmann DC (2009). Orthologs of Arabidopsis thaliana stomatal bHLH genes and regulation of stomatal development in grasses. Development 136, 2265-2276. DOI URL
[35]	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. DOI PMID
[36]	MacAlister CA, Ohashi-Ito K, Bergmann DC (2007). Transcription factor control of asymmetric cell divisions that establish the stomatal lineage. Nature 445, 537-540. DOI
[37]	Matos JL, Lau OS, Hachez C, Cruz-Ramírez A, Scheres B, Bergmann DC (2014). Irreversible fate commitment in the Arabidopsis stomatal lineage requires a FAMA and RETINOBLASTOMA-RELATED module. eLife 3, e03271. DOI URL
[38]	McKown KH, Bergmann DC (2020). Stomatal development in the grasses: lessons from models and crops (and crop models). New Phytol 227, 1636-1648. DOI URL
[39]	Miura K, Jin JB, Lee J, Yoo CY, Stirm V, Miura T, Ashworth EN, Bressan RA, Yun DJ, Hasegawa PM (2007). SIZ1-mediated sumoylation of ICE1 controls CBF3/ DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell 19, 1403-1414. DOI URL
[40]	Nadeau JA, Sack FD (2002). Control of stomatal distribution on the Arabidopsis leaf surface. Science 296, 1697-1700. DOI URL
[41]	Ohashi-Ito K, Bergmann DC (2006). Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development. Plant Cell 18, 2493-2505. DOI PMID
[42]	Pillitteri LJ, Sloan DB, Bogenschutz NL, Torii KU (2007). Termination of asymmetric cell division and differentiation of stomata. Nature 445, 501-505.
[43]	Pillitteri LJ, Torii KU (2012). Mechanisms of stomatal development. Annu Rev Plant Biol 63, 591-614. DOI PMID
[44]	Putarjunan A, Ruble J, Srivastava A, Zhao CZ, Rychel AL, Hofstetter AK, Tang XB, Zhu JK, Tama F, Zheng N, Torii KU (2019). Bipartite anchoring of SCREAM enforces stomatal initiation by coupling MAP kinases to SPEECHLESS. Nat Plants 5, 742-754. DOI PMID
[45]	Qu X, Peterson KM, Torii KU (2017). Stomatal development in time: the past and the future. Curr Opin Genes Dev 45, 1-9.
[46]	Raissig MT, Abrash E, Bettadapur A, Vogel JP, Bergmann DC (2016). Grasses use an alternatively wired bHLH transcription factor network to establish stomatal identity. Proc Natl Acad Sci USA 113, 8326-8331. DOI PMID
[47]	Raissig MT, Matos JL, Ximena Anleu Gil M, Kornfeld A, Bettadapur A, Abrash E, Allison HR, Badgley G, Vogel JP, Berry JA, Bergmann DC (2017). Mobile MUTE specifies subsidiary cells to build physiologically improved grass stomata. Science 355, 1215-1218. DOI PMID
[48]	Rudall PJ, Hilton J, Bateman RM (2013). Several developmental and morphogenetic factors govern the evolution of stomatal patterning in land plants. New Phytol 200, 598-614. DOI PMID
[49]	Serna L (2011). Stomatal development in Arabidopsis and grasses: differences and commonalities. Int J Dev Biol 55, 5-10. DOI URL
[50]	Serna L (2020). The role of grass MUTE orthologues during stomatal development. Front Plant Sci 11, 55. DOI URL
[51]	Wang HL, Guo SY, Qiao X, Guo JF, Li ZL, Zhou YS, Bai SL, Gao ZY, Wang DJ, Wang PC, Galbraith DW, Song CP (2019). BZU2/ZmMUTE controls symmetrical division of guard mother cell and specifies neighbor cell fate in maize. PLoS Genet 15, e1008377. DOI URL
[52]	Wei DH, Liu MJ, Chen H, Zheng Y, Liu YX, Wang X, Yang SH, Zhou MQ, Lin J (2018). INDUCER OF CBF EXPRESSION 1 is a male fertility regulator impacting anther dehydration in Arabidopsis. PLoS Genet 14, e1007695. DOI URL
[53]	Wu ZL, Chen L, Yu Q, Zhou WQ, Gou XP, Li J, Hou SW (2019). Multiple transcriptional factors control stomata development in rice. New Phytol 223, 220-232. DOI PMID
[54]	Ye KY, Li H, Ding YL, Shi YT, Song CP, Gong ZZ, Yang SH (2019). BRASSINOSTEROID-INSENSITIVE2 negatively regulates the stability of transcription factor ICE1 in response to cold stress in Arabidopsis. Plant Cell 31, 2682-2696.
[55]	Yoo CY, Pence HE, Jin JB, Miura K, Gosney MJ, Hasegawa PM, Mickelbart MV (2010). The Arabidopsis GTL1 transcription factor regulates water use efficiency and drought tolerance by modulating stomatal density via transrepression of SDD1. Plant Cell 22, 4128-4141. DOI URL
[56]	Zhou WQ, Wang YC, Wu ZL, Luo L, Liu P, Yan LF, Hou SW (2016). Homologs of SCAR/WAVE complex components are required for epidermal cell morphogenesis in rice. J Exp Bot 67, 4311-4323. DOI PMID
[57]	Zoulias N, Harrison EL, Casson SA, Gray JE (2018). Molecular control of stomatal development. Biochem J 475, 441-454. DOI PMID

玉米ZmICE2基因调控气孔发育

ZmICE2 Regulates Stomatal Development in Maize

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