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作物学报 ›› 2022, Vol. 48 ›› Issue (4): 825-839.doi: 10.3724/SP.J.1006.2022.14080

• 作物遗传育种·种质资源·分子遗传学 • 上一篇    下一篇

谷子糖转运蛋白基因SiSTPs的鉴定及其参与谷子抗逆胁迫响应的研究

晋敏姗1(), 曲瑞芳1, 李红英1,3, 韩彦卿2,3, 马芳芳1,3, 韩渊怀1,3, 邢国芳1,3,*()   

  1. 1山西农业大学农学院, 山西太谷 030801
    2山西农业大学植物保护学院, 山西太谷 030801
    3杂粮种质创新与分子育种山西省重点实验室, 山西太原 030000
  • 收稿日期:2021-04-28 接受日期:2021-07-12 出版日期:2022-04-12 网络出版日期:2021-08-11
  • 通讯作者: 邢国芳
  • 作者简介:E-mail: jms1995mashy@163.com
  • 基金资助:
    山西省重点研发计划项目(201803D221008-4);国家自然科学基金项目(32070366);山西省应用基础研究项目资助(201801D221298)

Identification of sugar transporter gene family SiSTPs in foxtail millet and its participation in stress response

JIN Min-Shan1(), QU Rui-Fang1, LI Hong-Ying1,3, HAN Yan-Qing2,3, MA Fang-Fang1,3, HAN Yuan-Huai1,3, XING Guo-Fang1,3,*()   

  1. 1College of Agronomy, Shanxi Agricultural University, Taigu 030801, Shanxi, China
    2College of Plant Protection, Shanxi Agricultural University, Taigu 030801, Shanxi, China
    3Shanxi Key Laboratory of Germplasm Innovation and Molecular Breeding of Minor Crop, Taiyuan 030000, Shanxi, China
  • Received:2021-04-28 Accepted:2021-07-12 Published:2022-04-12 Published online:2021-08-11
  • Contact: XING Guo-Fang
  • Supported by:
    Key Research and Development Program of Shanxi Province(201803D221008-4);National Natural Science Foundation of China(32070366);Applied Basic Research Project of Shanxi Province(201801D221298)

摘要:

糖转运蛋白(sugar transporter proteins, STPs)是一类主要转运己糖的单糖转运蛋白, 在作物的生长发育和抗逆过程中发挥着重要作用。谷子是绿色旱作农业的主栽作物, 也是C4光合作用机理和禾本科抗逆基因挖掘的模式植物, 目前有关谷子STP基因功能的研究还鲜有报道。因此, 本研究利用生物信息学方法, 对包括谷子在内的6种禾本科作物的STPs基因进行全基因组鉴定, 重点对谷子SiSTPs基因的理化性质、染色体定位、系统进化、基因结构、保守结构域、组织表达模式, 并对其参与谷子干旱和低磷胁迫以及白发病抗性响应进行了深入分析。在谷子、狗尾草、高粱、玉米、小麦和水稻中分别鉴定出STP基因家族成员24、26、23、22、33和27个, 系统进化分析聚为4类。谷子的24个SiSTP基因不均匀的分布在7条染色体上, 其编码氨基酸的大小为499~581 aa, 这些SiSTP蛋白都具有Sugar_tr (PF00083)保守结构域, 并且在启动子区存在大量的光响应以及逆境响应元件, 分析发现谷子SiSTPs基因在进化过程中受到了强烈的纯化选择压力, 存在明显的组织表达特异性, 且受光诱导, 不同成员在低磷胁迫、干旱胁迫和白发病侵染过程中表达存在差异。本研究为阐明谷子STP蛋白的功能以及响应逆境胁迫机理提供理论基础。

关键词: 谷子, 糖转运蛋白基因, 系统进化, 表达分析, 胁迫应答

Abstract:

Sugar transporter proteins (STPs), a class of monosaccharide transporters that mainly transport hexose, play an important role in the growth, development, and stress resistance of crops. Foxtail millet is the main cultivated crop in green dryland agriculture, and also is the model plant for C4 photosynthesis mechanism and stress resistance gene mining of Gramineae crops. However, no systematical study of SiSTPs gene has been performed in foxtail millet. In this study, we identified the whole genome of six Gramineae crops including foxtail millet by bioinformatics method, and focused on the physicochemical properties, the chromosomal localization, the systematic evolution, gene structure, and the conserved domain. Moreover, the relative expression level of SiSTPs gene and its resistance to the infection of Sclerospora graminicola under drought stress and low phosphate stress in foxtail millet were investigated. The results showed that a total of 24, 26, 23, 22, 33, and 27 STP gene family members were individually identified in Setaria italica, Setaria viridis, Sorghum bicolor, Zea mays, Triticum aestivum, and Oryza sativa, which were divided into four clades by phylogenetic analysis. The 24 SiSTP genes were distributed unevenly on 7 chromosomes, and the size of the encoded amino acids ranged from 499 aa to 581 aa. The SiSTP all had the Sugar_tr (PF00083) conserved domain. The cis-acting elements included a large number of light-responsive elements and stress-responsive elements. These SiSTPs was subjected to strong purification and selection pressure during the evolutionary process of foxtail millet, and had obvious tissue expression specificity and photoinduced phenomena. Different SiSTPs showed different temporal and spatial expression and response to the drought stress, the low phosphate stress, and Sclerospora graminicola infection. Our results provide a theoretical basis for elucidating the function and response mechanism to stress of SiSTP.

Key words: foxtail millet, sugar transporter proteins, systematic evolution, expression analysis, stress response

表1

本试验所用引物"

基因
Gene name
上游引物
Forward sequence (5′-3′)
下游引物
Reverse sequence (5'-3')
SiSTP4 ACCATGCTCTGCCACTTCAA TCTTCCAGAACCAGTGCGAC
SiSTP9 TGACATCGGCATCTCTGGTG GATGTTGAGCATCCCACGGA
SiSTP19 TGAAGTTCTTCCCGTCGGTG AGCTGGAACCCGATGTTGAG
SiSTP23 GACTTGCGGTCATCTCCCTC TGAGGCGACCTCTCTGATGA
β-Actin CAACAAGATGGATGCCACCAC GAGATTGGGACGAAGGCAATC

图1

谷子STPs基因的染色体定位"

表2

谷子STPs蛋白基本理化性质"

名称
Gene name
基因名称
Gene ID
氨基酸数目
Number of amino acids
等电点Isoelectric point 相对分子质量Molecular weight 不稳定指数
Instability index
脂肪系数Aliphatic index 平均疏水指数
Grand average of hydropathicity
SiSTP1 Seita.1G079800.1 520 9.10 57,150.45 36.01 101.27 0.596
SiSTP2 Seita.1G204900.1 525 8.77 56,604.51 45.82 105.52 0.619
SiSTP3 Seita.1G205000.1 518 9.34 55,004.35 38.13 105.83 0.619
SiSTP4 Seita.2G000400.1 516 8.36 56,378.41 34.38 102.46 0.523
SiSTP5 Seita.2G079100.1 506 9.34 55,238.58 37.97 96.03 0.414
SiSTP6 Seita.2G167300.1 522 9.13 55,270.80 37.54 100.00 0.552
SiSTP7 Seita.2G176800.1 504 9.06 54,941.45 33.51 107.56 0.528
SiSTP8 Seita.2G205100.1 520 9.41 56,007.80 39.32 105.04 0.512
SiSTP9 Seita.2G352200.1 527 9.20 57,372.78 31.35 106.41 0.579
SiSTP10 Seita.4G029600.1 529 9.75 56,006.24 34.25 102.76 0.497
SiSTP11 Seita.5G204000.1 509 9.44 55,305.53 37.53 109.39 0.698
SiSTP12 Seita.6G043500.1 499 6.52 53,829.04 36.97 106.23 0.650
SiSTP13 Seita.7G007500.1 513 9.47 55,508.58 34.04 110.84 0.707
SiSTP14 Seita.7G119800.1 512 9.81 55,140.95 31.73 100.27 0.574
SiSTP15 Seita.7G120000.1 513 9.73 55,566.19 38.80 100.94 0.545
SiSTP16 Seita.7G120100.1 512 8.97 55,632.07 36.42 103.98 0.569
SiSTP17 Seita.7G120200.1 514 9.32 55,147.58 36.22 104.40 0.572
SiSTP18 Seita.7G120300.1 534 9.91 57,645.50 38.48 99.23 0.432
SiSTP19 Seita.7G120800.1 511 9.67 53,895.89 31.18 102.97 0.611
SiSTP20 Seita.9G122300.1 520 9.41 55,987.81 39.48 105.98 0.518
SiSTP21 Seita.9G187300.1 525 9.19 56,067.71 33.69 104.82 0.581
SiSTP22 Seita.9G322100.1 516 9.51 57,307.68 45.13 108.66 0.466
SiSTP23 Seita.9G488700.1 581 9.36 64,227.29 34.11 107.02 0.399
SiSTP24 Seita.9G579300.1 516 9.19 56,549.60 38.76 109.75 0.567

表3

谷子STPs蛋白二级结构预测和亚细胞定位"

序号
Number
名称
Gene name
α-螺旋 α-helix (%) 延伸链 Extended strand (%) β-折叠 β-turn (%) 无规则卷曲Random coil (%) 亚细胞定位
Subcellular localization
保守结构域
Domain
1 SiSTP1 52.12 15.96 4.62 27.31 细胞质膜Plasma membrane MFS_STP
2 SiSTP2 48.57 16.38 5.71 29.33 细胞质膜Plasma membrane MFS_STP
3 SiSTP3 51.16 15.25 4.83 28.76 细胞质膜Plasma membrane MFS_STP
4 SiSTP4 50.39 16.09 6.59 26.94 细胞质膜Plasma membrane MFS_STP
5 SiSTP5 50.59 16.40 4.55 28.46 细胞质膜Plasma membrane MFS_STP
6 SiSTP6 49.62 15.71 5.36 29.31 细胞质膜Plasma membrane MFS_STP
7 SiSTP7 50.40 16.47 5.36 27.78 细胞质膜Plasma membrane MFS_STP
8 SiSTP8 47.31 16.54 5.58 30.58 细胞质膜Plasma membrane MFS_STP
9 SiSTP9 50.09 16.51 5.31 28.08 细胞质膜Plasma membrane MFS_STP
10 SiSTP10 48.96 17.39 4.73 28.92 细胞质膜Plasma membrane MFS_STP
11 SiSTP11 47.15 17.49 4.72 30.65 细胞质膜Plasma membrane MFS_STP
12 SiSTP12 51.70 16.23 5.41 26.65 细胞质膜Plasma membrane MFS_STP
13 SiSTP13 50.29 17.35 4.68 27.68 细胞质膜Plasma membrane MFS_STP
14 SiSTP14 49.41 16.99 4.88 28.71 细胞质膜Plasma membrane MFS_STP
15 SiSTP15 51.46 15.40 5.46 27.68 细胞质膜Plasma membrane MFS_STP
16 SiSTP16 51.17 16.02 4.88 27.93 细胞质膜Plasma membrane MFS_STP
17 SiSTP17 51.17 16.73 5.64 26.46 细胞质膜Plasma membrane MFS_STP
18 SiSTP18 47.00 13.86 4.68 34.46 细胞质膜Plasma membrane MFS_STP
19 SiSTP19 49.32 16.44 5.68 28.75 细胞质膜Plasma membrane MFS_STP
20 SiSTP20 47.12 16.92 5.38 30.58 细胞质膜Plasma membrane MFS_STP
21 SiSTP21 51.05 15.62 5.71 27.62 细胞质膜Plasma membrane MFS_STP
22 SiSTP22 53.10 15.31 4.46 27.13 细胞质膜Plasma membrane MFS_STP
23 SiSTP23 45.96 15.83 5.68 32.53 细胞质膜Plasma membrane MFS_STP
24 SiSTP24 50.00 16.28 6.20 27.52 细胞质膜Plasma membrane MFS_STP

图2

谷子与其他作物的STP基因家族成员的系统进化树 SiSTP1~SiSTP24为谷子STP家族成员(红色); SvSTP1~SvSTP26为青狗尾草STP家族成员; SbSTP1~SbSTP23为高粱STP家族成员; ZmSTP1~ZmSTP22为玉米STP家族成员; TaSTP1~TaSTP33小麦STP家族成员; OsSTP1~OsSTP27水稻STP家族成员。"

表4

谷子STPs基因家族成员15个蛋白基序分析"

基序
Motif
序列
Sequence
长度
Width (aa)
所在基因个数
Number of genes
Motif 1 LCAFKYGIFLFFAAWVVVMTVFVAAFLPETKGVPJEEM 38 24
Motif 2 NGAAVNVAMLIVGRILLGVGVGFTNQAVPLYLSEMAPARWRGALNIGFQL 50 24
Motif 3 QYCKYDSQLLTAFTSSLYLAGLVASLVASRVTRRFGRKASM 41 24
Motif 4 CVYVAGFGWSWGPLGWLVPSEIFPLEIRS 29 24
Motif 5 DYGGKVTFFVVLTCLVAASGGLIFGYDIGISGGVTSMDPFLKKFFPEVYR 50 23
Motif 6 IPVFQQLTGINVIMFYAPVLFRTVGFGSDA 30 24
Motif 7 WGWRLSLGLAAVPAAVITLGALFLPDTPNSLILR 34 23
Motif 8 VSIVTVDRLGRRKLFLQGGAQMJICQVAVGWILGAKFGASG 41 24
Motif 9 RLVWRRHWYWKRFVRDEPDEA 21 24
Motif 10 FRNJLRRRYRPQLVM 15 24
Motif 11 FITJGILAANLINYGTNKIPG 21 23
Motif 12 DVDAEFKDJVAASEEARAVEH 21 24
Motif 13 NLLFTFVIAQAFLSM 15 24
Motif 14 GRPDEARAVLQRIRG 15 23
Motif 15 SLMSAVITGLVNLFA 15 23

图3

谷子STPs基因结构和保守结构域分析"

图4

谷子STPs基因家族成员启动子顺式作用元件预测"

图5

谷子、水稻和拟南芥的糖转运蛋白基因STPs共线性分析"

表5

SiSTP、OsSTP、AtSTP基因进化选择压力分析"

比对基因_1
Gene_1
比对基因_2
Gene_2
非同义替换
Ka
同义替换
Ks
非同义替换/同义替换
Ka/Ks
SiSTP1 OsSTP3 0.11781299 0.32157912 0.36635770
SiSTP3 OsSTP12 0.33694743 0.60239717 0.55934430
SiSTP4 OsSTP17 0.09187094 0.37007634 0.24824862
SiSTP5 OsSTP20 0.13761001 0.47474108 0.28986328
SiSTP6 OsSTP24 0.13021302 0.34325476 0.37934802
SiSTP8 OsSTP25 0.04544091 0.23400541 0.19418743
SiSTP9 OsSTP21 0.04068573 0.31030313 0.13111608
SiSTP10 OsSTP16 0.10871793 0.30090572 0.36130230
SiSTP11 OsSTP1 0.10108616 0.28074655 0.36006199
SiSTP12 OsSTP22 0.07095251 0.33044715 0.21471666
SiSTP15 OsSTP13 0.21042393 0.38939049 0.54039311
SiSTP17 OsSTP6 0.37053540 0.62711506 0.59085712
SiSTP23 OsSTP8 0.03796308 0.30304824 0.12527075
SiSTP24 OsSTP7 0.11469825 1.12797658 0.10168496
SiSTP9 AtSTP1 0.26072995 3.45057903 0.07556122
SiSTP9 AtSTP12 0.32117875 2.34003570 0.13725378

图6

谷子STPs基因在不同组织部位表达分析 Seed_30、60-days-after-maturation为成熟后30、60 d种子; Immature-seed_S1、S2、S3、S4、S5分别为S1~S5时期未成熟时期种子; Immature-spikelet_S2、S4为S2和S4时期未成熟穗; Panicle_Primary-panicle-branch-differentiation-stage为初穗分枝分化期穗部; Panicle_Third-panicle-branch-differentiation-stage第3穗分枝分化期穗部; Root_Filling-stage为灌浆期根; Germinated-seeds_3-days为发芽3 d幼苗; Plant_one-tip-two-leaf为两叶一心期幼苗; Flag-leaf_filling-stage为灌浆期旗叶; Leaf-top-foruth_filling-stage为灌浆期第4叶; Flag-leaf-sheath_filling-stage为灌浆期旗叶鞘Leaf-sheath-top-foruth_filling-stage为灌浆期第4片顶叶叶鞘; Leaf-top-2-3_ 2-days-after-heading为抽穗2 d后2~3片顶叶; Neck-panicle-internodes_Filling-stage灌浆期穗颈; Stem-top-second_Filling-stage为灌浆期第2节茎。"

图7

谷子STPs基因在非生物胁迫下的表达分析 图A为低磷胁迫表达分析, 其中0 h、2 h、12 h分别代表取样时间为处理0、2、12 h; NP、LP分别代表正常磷处理和低磷处理。Overground part、Root分别代表取样部位为地上部和根系。图B为干旱胁迫表达分析, 其中Control、Drought分别代表对照组和干旱处理组; R、S分别代表抗旱品种和干旱敏感品种。M、N、E分别代表不同取样时间和光照: (早)中等光照、(午)强光照、(晚)弱光照。"

图8

谷子STPs基因在白发病侵染后胁迫下的表达分析 Control、Downy mildew分别代表对照组和白发病菌侵染处理组; R、S分别代表抗病品种和感病品种; 3、5、7分别代表不同取样时间三叶期、五叶期和七叶期。"

图9

低磷、干旱、白发病侵染胁迫下SiSTP4、SiSTP9、SiSTP19、SiSTP23基因的相对表达量 A为低磷胁迫; B为干旱胁迫; C为白发病侵染。缩写同图7和图8。"

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