利用RNA-Seq发掘玉米叶片形态建成相关的调控基因

doi:10.3864/j.issn.0578-1752.2020.01.001

Abstract

Abstract:

【Objective】Leaf shape characteristics are one of important agronomic traits that determine plant morphology and affect planting density. However, the molecular mechanism related to leaf shape remain unknown in maize. Here, transcriptome sequencing technology was used to screen and explore genome-wide analysis of regulatory genes and metabolic pathways involved in leaf morphogenesis. This study will lay the foundation for further understanding the regulator mechanism of leaf development in plant and identifying candidate genes of leaf shapes, such as leaf width and leaf length.【Method】 Extreme narrow-leaf inbred line NL409 and wide-leaf line WB665 were selected as the experimental materials. By RNA-Seq technology, the differentially expressed genes (DEGs) of the seventh leaf base between these two lines were identified during the 7th leaf stage. Furthermore, metabolic pathways closely related to leaf development were also analyzed using a series of bioinformatics analysis. qRT-PCR was used to validate the expression level of DEGs in different hormone pathways, and the further promoter analysis were performed to explore leaf-shape functional genes.【Result】By analyzing the high-throughput sequencing in WB665 and NL409, a total of 5 199 DEGs were obtained at the primary section of leaf width formation. Of which, 2 264 (43.55%) genes were up-regulated, whereas down-regulated genes were significantly more than up-regulated genes with 2 935 (56.45%) decreased genes. GO enrichment analysis showed that these DEGs were mainly enriched in cell membrane-associated function terms of cellular components, including metabolic process and cell stimulus response. KEGG enrichment analysis showed that these DEGs were mainly involved in ribosome, plant hormone signal transduction, sphingolipid metabolism pathways, phenylpropanoid biosynthesis, glyoxylate and dicarboxylate metabolism and other processes. among which ribosome, plant hormone signal transduction, sphingolipid metabolism pathways with more down-regulated genes were closely related to leaf development. One of PRS (PRESSED FLOWER) family genes, which were enriched in the ribosomal pathway in this study, PRS13 (PFL2) was identified to participate in regulating the development of narrow leaves. The expression pattern of genes enriched in sphingolipid metabolism pathway and its related MAP kinase, AP1-like, and LFY-like were consistent with the result of the inhibited development of narrow leaves. Notably, all of BR (Brassinosteroid) response genes and most of GA (Gibberellin) metabolic genes were down-regulated in plant hormone signal transduction pathway, while the expression level of all the CTK (Cytokinine) response genes and Auxin genes are mostly increased. The action of up-regulated expression of DELLA protein gene affecting the GA and CTK pathways was consistent with the phenotypic result of narrow leaves. Eighteen genes were validated by qRT-PCR. The result showed that the expression trend was consistent with the transcriptome data. Moreover, the BR-related ROT3, auxin-related NAL7-like, AGO7-like and TCP-like transcription factors CYC/TB1 were identified to be closely associated with the formation of narrow leaves.【Conclusion】Summarily, this study unveils several metabolic pathways closely related to leaf development in maize, and find the dynamic balance between plant hormones plays an important role in leaf development, especially the interaction between Auxin and BR as well as CTK and GA.

Key words: maize (Zea mays), leaf width, leaf length, RNA-Seq, morphogenesis, regulatory gene

ShuLei GUO,XiaoMin LU,JianShuang QI,LiangMing WEI,Xin ZHANG,XiaoHua HAN,RunQing YUE,ZhenHua WANG,ShuangGui TIE,YanHui CHEN. Explore Regulatory Genes Related to Maize Leaf Morphogenesis Using RNA-Seq[J].Scientia Agricultura Sinica, 2020, 53(1): 1-17.

Figures/Tables 12

Fig. 1

Table 1

Table 2

Fig. 2

Fig. 3

Fig. 4

Fig. 5

Table 3

Table 4

Sphingolipid metabolism pathway and related genes"

路径 pathway	基因编号 Gene ID	差异倍数 FC		基因描述/注释 Gene description/annotation
鞘脂类代谢 Sphingolipid metabolism	GRMZM2G165613	0.00	下调Down	丝氨酸软脂酰转移酶,长链碱基生物合成蛋白1b Serine palmitoyltransferase, Long chain base biosynthesis protein 1b
	GRMZM2G444378	0.00	下调Down	丝氨酸软脂酰转移酶,PKC激活蛋白磷酸酶1型抑制剂 Serine palmitoyltransferase, PKC-activated protein phosphatase-1 inhibitor
	GRMZM2G449763	0.00	下调Down	丝氨酸软脂酰转移酶,胺核黄素氧化还原酶 Serine palmitoyltransferase, Flavin containing amine oxidoreductase
	GRMZM2G076398	0.00	下调Down	丝氨酸软脂酰转移酶,长链碱基生物合成蛋白1b Serine palmitoyltransferase, Long chain base biosynthesis protein 1b
	GRMZM2G134248	0.24	下调Down	丝氨酸软脂酰转移酶,长链碱基生物合成蛋白1b Serine palmitoyltransferase, Long chain base biosynthesis protein 1b
	GRMZM2G144985	0.33	下调Down	丝氨酸软脂酰转移酶,长链碱基生物合成蛋白1b Serine palmitoyltransferase, Long chain base biosynthesis protein 1b
	GRMZM2G152888	0.30	下调Down	丝氨酸软脂酰转移酶,长链碱基生物合成蛋白2a Serine palmitoyltransferase, Long chain base biosynthesis protein 2a
	GRMZM2G357734	0.02	下调Down	丝氨酸软脂酰转移酶,胺核黄素氧化还原酶 Serine palmitoyltransferase, Flavin containing amine oxidoreductase
	GRMZM2G402368	0.01	下调Down	SUR2,鞘氨醇C4型单加氧酶2 SUR2, sphinganine C4-monooxygenase 2
	GRMZM2G030118	0.11	下调Down	SUR2,鞘氨醇C4型单加氧酶2 SUR2, sphinganine C4-monooxygenase 2
	GRMZM2G346455	0.46	下调Down	α-半乳糖苷酶,参与植物细胞壁 Alpha-galactosidase 1, involved in plant-type cell wall
	GRMZM2G095126	2.66	上调Up	α-半乳糖苷酶,参与植物细胞壁 Alpha-galactosidase 1, involved in plant-type cell wall
	GRMZM2G105922	2.27	上调Up	GBA2,非溶酶体葡糖神经酰胺酶 GBA2, non-lysosomal glucosylceramidase
MAP激酶 MAP kinase	GRMZM2G135904	13.57	上调Up	MAPK12,丝裂原激活蛋白激酶家族蛋白 MAPK12, MAP kinase family protein
	GRMZM2G459824	8.117	上调Up	MAPKKK2,丝裂原激活蛋白激酶激酶激酶ANP1 MAPKKK2, MAP kinase kinase kinase ANP1-like
	GRMZM5G878379	3.00	上调Up	MAPKK4,丝裂原激活蛋白激酶家族蛋白 MAPKK4, MAP kinase family protein
	GRMZM2G064601	2.49	上调Up	MAPKKK,丝裂原激活蛋白激酶激酶激酶YODA MAPKKK, MAP kinase kinase kinase YODA
	GRMZM2G062761	2.04	上调Up	MAPK17,丝裂原激活蛋白激酶家族蛋白 MAPK17, MAP kinase family protein
AP1类 AP1-like	GRMZM2G055782	17.58	上调Up	MADS-box型转录因子27 MADS-box transcription factor 27-like
	GRMZM2G147716	3.78	上调Up	AGL8/AP1,K-box和MADS-box型转录因子家族 AGL8/AP1, K-box region and MADS-box transcription factor family
	GRMZM2G070034	2.88	上调Up	MADS-box型转录因子56 MADS-box transcription factor 56-like
LFY 类LFY-like	GRMZM2G162814	0.25	下调Down	多叶,花分生组织蛋白,影响花和叶片的发育 Leafy, floral meristem identity protein, affect flower and leaf development

Table 4

Table 5

Some genes related to plant hormone signal transduction"

激素 Hormones	基因编号 Gene ID	差异倍数 FC（T7/C7）		基因描述/注释 Gene description/annotation
生长素信号 Auxin signaling	GRMZM2G030710	3.38	上调Up	ARF,类生长素响应因子15,调控转录 ARF, Auxin response factor 15-like, regulation of transcription
	GRMZM2G078274	2.54	上调Up	ARF,类生长素响应因子3,调控转录 ARF, Auxin response factor 3-like, regulation of transcription
	GRMZM5G874163	2.07	上调Up	ARF,类生长素响应因子3,激活生长素信号通路 ARF, Auxin response factor 3-like, auxin-activated signaling pathway
	GRMZM2G361376	0.00	下调Down	ARF,类生长素响应因子15,细胞响应生长素刺激 ARF, Auxin response factor 15-like, cellular response to auxin stimulus
	GRMZM5G853479	70.68	上调Up	生长素响应蛋白IAA4,细胞响应生长素刺激 Auxin-responsive protein IAA4, cellular response to auxin stimulus
	GRMZM2G104176	7.53	上调Up	生长素响应蛋白IAA2,激活生长素信号通路 Auxin-responsive protein IAA2, auxin-activated signaling pathway
	GRMZM2G077356	4.12	上调Up	生长素响应蛋白IAA13,激活生长素信号通路 Auxin-responsive protein IAA13, auxin-activated signaling pathwa
	GRMZM2G079957	3.86	上调Up	生长素响应蛋白IAA31,激活生长素信号通路 Auxin-responsive protein IAA31, auxin-activated signaling pathway
	GRMZM2G074427	0.12	下调Down	生长素响应蛋白IAA18,细胞响应生长素刺激 Auxin-responsive protein IAA18, cellular response to auxin stimulus
	GRMZM2G079200	0.01	下调Down	生长素响应蛋白IAA23,激活生长素信号通路 Auxin-responsive protein IAA23, auxin-activated signaling pathway
	GRMZM2G059544	0.02	下调Down	生长素响应蛋白IAA25,细胞响应生长素刺激 Auxin-responsive protein IAA25, cellular response to auxin stimulus
	GRMZM2G429254	4.12	上调Up	SAUR家族生长素响应蛋白SAUR32,生长素代谢 SAUR family auxin-responsive protein SAUR32, auxin metabolism
	GRMZM2G391596	3.46	上调Up	SAUR家族生长素响应蛋白SAUR36,生长素代谢 SAUR family auxin-responsive protein SAUR36, auxin metabolism
	GRMZM2G361993	0.34	下调Down	SAUR家族生长素响应蛋白SAUR32,生长素代谢 SAUR family auxin-responsive protein SAUR32, auxin metabolism
	GRMZM2G475683	0.24	下调Down	SAUR家族生长素响应蛋白SAUR12,生长素代谢 SAUR family auxin-responsive protein SAUR12, auxin metabolism
	GRMZM2G410567	2.35	上调Up	生长素响应GH3基因家族,响应生长素刺激 Auxin-responsive GH3 gene family, response to auxin stimulus
	GRMZM2G067022	4.17	上调Up	AUX1,类生长素转运蛋白1,跨膜转运体 AUX1, Auxin transporter-like protein 1, transmembrane transporter
	GRMZM2G127949	2.00	上调Up	AUX1,类生长素转运蛋白1,跨膜转运体 AUX1, Auxin transporter-like protein 1, transmembrane transporter
油菜素内酯信号BR signaling	GRMZM2G158775	0.39	下调Down	BRI1,油菜素内酯不敏感1,膜受体,激活BZR1 BRI1, brassinosteroid insensitive 1, membrane receptor, activation of BZR1
	AC194970.5_FG002	0.27	下调Down	BZR1,芸苔素唑拮抗1,油菜素内酯信号转导 BZR1, brassinazole-resistant 1, brassinosteroid signal transduction
	GRMZM2G127050	0.49	下调Down	BSK,油菜素内酯信号激酶,膜受体,BRI1激酶底物 BSK, BR-signaling kinase, membrane receptor, substrates of BRI1 kinase
	GRMZM2G164224	0.31	下调Down	BSK,油菜素内酯信号激酶,膜受体,BRI1激酶底物 BSK, BR-signaling kinase, membrane receptor, substrates of BRI1 kinase
	GRMZM2G054634	0.17	下调Down	BSK,油菜素内酯信号激酶,膜受体,BRI1激酶底物 BSK, BR-signaling kinase, membrane receptor, substrates of BRI1 kinase
	AC210669.3_FG001	0.05	下调Down	木葡聚糖转移酶TCH4,细胞伸长和扩展 Xyloglucosyl transferase TCH4, cell elongation and expansion
油菜素内酯合成BR biosynthesis	GRMZM2G103773	11.89	上调Up	油菜素内酯-6-氧化酶2,细胞膜固有成分 Brassinosteroid-6-oxidase 2, intrinsic component of membrane
	GRMZM2G107199	5.83	上调Up	D11,细胞色素P450,细胞膜固有成分,氧化还原活性 D11, cytochrome P450, integral component of membrane, oxidoreductase activity
	GRMZM2G143235	5.57	上调Up	D2,类固醇3-氧化酶,细胞膜部分,氧化还原活性 D2, steroid 3-oxidase, membrane part, oxidoreductase activity
	GRMZM2G032896	2.78	上调Up	D2,类固醇3-氧化酶,细胞膜固有成分,氧化还原活性 D2, steroid 3-oxidase, intrinsic component of membrane, oxidoreductase activity
	GRMZM2G065635	0.35	下调Down	DWF4,类固醇22-α-羟化酶,细胞膜固有成分 DWF4, steroid 22-alpha-hydroxylase, intrinsic component of membrane
	GRMZM2G162737	0.04	下调Down	CPD,细胞色素P450,细胞膜固有成分,氧化还原活性 CPD, cytochrome P450, integral component of membrane, oxidoreductase activity
	GRMZM5G872368	0.03	下调Down	BR6OX2,油菜素内酯-6-氧化酶2,细胞膜固有成分 BR6OX2, brassinosteroid-6-oxidase 2, intrinsic component of membrane
细胞分裂素信号CTK signaling	GRMZM5G884914	73.11	上调Up	双组分响应调节器ARR-B家族,响应刺激 Two-component response regulator ARR-B family, response to stimulus
	GRMZM2G409974	2.32	上调Up	双组分响应调节器ARR-B家族,响应刺激 Two-component response regulator ARR-B family, response to stimulus
	GRMZM2G013612	2.11	上调Up	类双组分响应调节器ARR-10,调控转录 Two-component response regulator ARR10-like, regulation of transcription
赤霉素信号GAs	GRMZM2G013016	6.80	上调Up	GAI1型DELLA蛋白,膜上细胞器,信号转导 DELLA protein GAI1-like, membrane-bounded organelle, signal transduction
赤霉素代谢相关基因 GAmrg	GRMZM2G073779	0.38	下调Down	GRAS家族参与赤霉素代谢,调控植株生长与发育 GRAS family, as a player in GA metabolism, regulate plant growth and development
	GRMZM2G073805	0.29	下调Down	GRAS家族参与赤霉素代谢,调控植株生长与发育 GRAS family, as a player in GA metabolism, regulate plant growth and development
	GRMZM2G098517	0.23	下调Down	GRAS家族参与赤霉素代谢,调控植株生长与发育 GRAS family, as a player in GA metabolism, regulate plant growth and development
	GRMZM2G018254	0.04	下调Down	GRAS家族参与赤霉素代谢,调控植株生长与发育 GRAS family, as a player in GA metabolism, regulate plant growth and development
	GRMZM2G070371	0.00	下调Down	GRAS家族参与赤霉素代谢,调控植株生长与发育 GRAS family, as a player in GA metabolism, regulate plant growth and development
	GRMZM2G110579	3.02	上调Up	GRAS家族参与赤霉素代谢,调控植株生长与发育 GRAS family, as a player in GA metabolism, regulate plant growth and development
	GRMZM2G036340	0.42	下调Down	GA 3氧化酶1,赤霉素3-β-双加氧酶活性 GA 3-oxidase 1, gibberellin 3-beta-dioxygenase activity
	GRMZM2G006964	0.3	下调Down	GA 2氧化酶6,赤霉素2-β-双加氧酶活性 GA 2-oxidase 6, gibberellin 2-beta-dioxygenase activity
	GRMZM2G323504	0.37	下调Down	GA受体GID1L2,羟基亚甲丁酸吡喃葡糖转化酶 GA receptor GID1L2, tuliposide A-converting enzyme
	GRMZM2G049675	0.29	下调Down	GA受体GID1L2,羟基亚甲丁酸吡喃葡糖转化酶 GA receptor GID1L2, tuliposide A-converting enzyme
	GRMZM2G156310	0.09	下调Down	GA受体GID1L2,羟基亚甲丁酸吡喃葡糖转化酶 GA receptor GID1L2, tuliposide A-converting enzyme
	AC203966.5_FG005	0.21	下调Down	GA 20氧化酶1,调控叶形和矮化 GA 20 oxidase 1, regulate leaves shape and dwarfism

Table 5

Fig. 6

Fig. 7

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材料¹⁾ Material	叶宽 Leaf width (cm)	叶长 Leaf length (cm)	叶面积 Leaf area (cm²)
NL409-7	2.49±0.13A	36.44±2.92A	66.12±8.59A
WB665-7	4.26±0.34B	29.67±1.67B	89.44±12.45B
NL409-S	4.67±0.27A	65.47±2.47A	223.31±13.11A
WB665-S	10.88±0.58B	59.89±2.57B	475.60±24.80B

样品¹⁾ Sample	原始序列 Raw reads	过滤后序列 Clean reads	高质量序列 Clean reads (%)	比对到基因组序列 Mapped reads	锚定比例 Mapped (%)	单一位置序列 Unique mapped reads (%)	过滤后Q30比例 Q30 after filter (%)
NL409-71	48570184	47805714	98.43	38240306	79.99	77.12	93.19
NL409-72	45215054	44236906	97.84	34918002	78.93	76.23	92.06
NL409-73	46822340	46156716	98.58	37211749	80.62	77.79	95.02
WB665-71	45625722	44792028	98.17	34166045	77.96	73.34	92.53
WB665-72	43848894	43120278	98.34	33618206	78.80	75.21	94.68
WB665-73	47838874	47202952	98.67	37193868	78.02	76.00	95.38

代谢通路 Pathway	代谢通路ID Pathway ID	差异基因数目 Counts of DEGs	P值 P-value
油菜素内酯生物合成Brassinosteroid biosynthesis	map00905	7	0.00088
乙醛酸和二羧酸代谢Glyoxylate and dicarboxylate metabolism	map00630	25	0.00108
核糖体Ribosome	map03010	83	0.00464
苯丙烷类代谢Phenylpropanoid biosynthesis	map00940	33	0.00854
植物激素信号转导Plant hormone signal transduction	map04075	57	0.01099
苯并恶嗪类生物合成Benzoxazinoid biosynthesis	map00402	7	0.02726
谷胱甘肽代谢Glutathione metabolism	map00480	23	0.02847
鞘脂类代谢Sphingolipid metabolism	map00600	13	0.03916
二萜类生物合成Diterpenoid biosynthesis	map00904	6	0.04792
类黄酮生物合成Flavonoid biosynthesis	map00941	8	0.04716
苯乙烯类、二芳庚酸类和姜酚类生物合成Stilbenoid, diarylheptanoid and gingerol biosynthesis	map00945	7	0.04825

Explore Regulatory Genes Related to Maize Leaf Morphogenesis Using RNA-Seq

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