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作物学报 ›› 2023, Vol. 49 ›› Issue (8): 2105-2121.doi: 10.3724/SP.J.1006.2023.24194

• 作物遗传育种·种质资源·分子遗传学 • 上一篇    下一篇

谷子HAK/KUP/KT钾转运蛋白家族全基因组鉴定及其对低钾和高盐胁迫的响应

代书桃1(), 朱灿灿1, 马小倩2, 秦娜1, 宋迎辉1, 魏昕1, 王春义1, 李君霞1,*()   

  1. 1 河南省农业科学院粮食作物研究所, 河南郑州 450002
    2 河南科技大学农学院, 河南洛阳 471023
  • 收稿日期:2022-08-24 接受日期:2023-02-10 出版日期:2023-08-12 网络出版日期:2023-02-21
  • 通讯作者: 李君霞
  • 作者简介:E-mail: daist82@163.com
  • 基金资助:
    财政部和农业农村部国家现代农业产业技术体系建设专项(CARS-06-14.5-B24);河南省良种联合攻关项目(2022010401);中央引导地方科技发展资金(Z20221341070);河南省农业科学院创新团队和自主创新项目(TD2022033);河南省农业科学院创新团队和自主创新项目(2022ZC07)

Genome-wide identification of the HAK/KUP/KT potassium transporter family in foxtail millet and its response to K+ deficiency and high salt stress

DAI Shu-Tao1(), ZHU Can-Can1, MA Xiao-Qian2, QIN Na1, SONG Ying-Hui1, WEI Xin1, WANG Chun-Yi1, LI Jun-Xia1,*()   

  1. 1 Cereal Crops Institute, Henan Academy of Agricultural Sciences, Zhengzhou 450002, Henan, China
    2 College of Agriculture, Henan University of Science and Technology, Luoyang 471023, Henan, China
  • Received:2022-08-24 Accepted:2023-02-10 Published:2023-08-12 Published online:2023-02-21
  • Contact: LI Jun-Xia
  • Supported by:
    China Agriculture Research System of MOF and MARA(CARS-06-14.5-B24);Funding of Joint Research on Agricultural Varieties Improvement of Henan Province(2022010401);Central Guidance on Science and Technology Development of Henan(Z20221341070);Innovation Team and Independent innovation Project of Henan Academy of Agricultural Sciences(TD2022033);Innovation Team and Independent innovation Project of Henan Academy of Agricultural Sciences(2022ZC07)

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摘要：

KT/HAK/KUP (HAK)家族是植物中最丰富的钾转运体家族, 对植物的生长和环境适应具有重要作用。谷子是抗逆耐瘠研究的模式植物, 然而, 谷子中HAK家族缺乏系统研究。本研究基于基因组序列信息, 鉴定出29个谷子HAK基因(SiHAKs), 并对该家族成员的基本特征、蛋白结构、染色体定位、基因复制、表达模式和逆境响应等方面进行了系统分析。结果显示, (1) SiHAKs分为5个进化簇(Cluster I~Cluster V), 成员数量分别为11、9、3、3和3。基因结构和蛋白保守基序分析表明, 谷子HAK家族具有较高的保守性, 不同Cluster的保守性依次为: Cluster III = Cluster V > Cluster II > Cluster I > Cluster IV。(2) 串联复制是SiHAKs扩增的主要原因, 15个SiHAKs位于串联重复中。(3) 171个转录因子可能结合到不同SiHAKs的启动子上, 这些转录因子包含ERF、NAC、MYB和WRKY等家族中的大量成员, 可能授予了SiHAKs对非生物胁迫多样的响应机制。(4) 基因表达聚类将SiHAKs分成3组: Group I、Group II和Group III, 多数SiHAKs在张谷和豫谷1号2个品种中的表达模式具有一致性; 不同Cluster表达水平总体表现为: Cluster III > Cluster V > Cluster II > Cluster I > Cluster IV。(5) 根系中表达水平较高的11个SiHAKs用来检测对低钾和高盐胁迫的响应。在低钾胁迫后, 8个SiHAKs的表达水平显著升高, 1个SiHAK显著降低, 2个SiHAKs变化不明显; 而高盐胁迫后, 3个SiHAKs的表达水平显著升高, 2个SiHAKs显著降低, 其余6个SiHAKs变化不明显。SiHAK15受到低钾和高盐胁迫的响应最为强烈, 其表达量分别为对照的151倍和22倍。(6) 基因表达谱的差异反映出不同Cluster间SiHAKs的功能差异。Cluster I主要在根系中表达, 可能参与谷子根系K+的吸收; Cluster II不具有组织表达特异性, 推测其参与K+的吸收、转运和生长发育等多个生物过程; Cluster III受到低钾和高盐2种胁迫的诱导, 显示出维持谷子K+/Na+平衡和抵御盐胁迫的潜在作用; Cluster IV在被检测的多个组织中几乎不表达; Cluster V不同成员对低钾和高盐胁迫的响应存在差异, 可能发生了功能分化。研究结果不仅为深入解析谷子HAK家族的功能奠定了基础, 而且为植物中钾高效利用和耐盐机制的研究提供了重要线索。

关键词: 谷子, 钾转运蛋白, KT/HAK/KUP家族, 盐胁迫, 表达分析

Abstract:

KT/HAK/KUP (HAK) family is the most abundant potassium (K+) transporter family in plants, which plays important roles in plant growth and environmental adaptation. Foxtail millet (Setaria italic L. Beauv) is a model plant for studies on stress resistance mechanisms. However, the HAK family has not yet been well characterized in foxtail millet. In this study, 29 Setaria italic HAK genes (SiHAKs) were identified based on genome-wide sequence information, and the basic characteristics, protein structure, chromosome location, gene replication, expression pattern, and responses to stress were comprehensively analyzed. The results showed as followes: (1) SiHAKs were divided into five phylogenetic clusters (Cluster I-Cluster V), containing 11, 9, 3, 3 and 3 members, respectively. Gene structure and conserved motif analyses indicated that SiHAKs was high conserved, and the conservatisms were as follows: Cluster III = Cluster V > Cluster II > Cluster I > Cluster IV. (2) Tandem replication was the main contribution to the amplification of SiHAKs. 15 SiHAKs were located in tandem replication. (3) 171 transcription factors, including a large number of members of ERF, NAC, MYB and WRKY families, may bind to the promoter sequences of SiHAKs, which may confer SiHAKs diverse response mechanisms to abiotic stress. (4) SiHAKs were divided into three groups (Group I, Group II, and Group III) by gene expression Cluster Ing. The relative expression patterns of most SiHAKs were consistent in the two varieties (Zhanggu and Yugu 1). The relative expression levels of SiHAKs from the five clusters were generally as follows: Cluster III > Cluster V > Cluster II > Cluster I> Cluster IV. (5) Eleven SiHAKs with high expression levels in root were selected to detect the responses to low K+ and high salt stress. Under K+ deficiency treatment, eight SiHAKs were markedly upregulated in the expression levels, one SiHAK was significantly decreased, and two SiHAKs had no obvious changes. Under high salt stress, Three SiHAKs were significantly increased in the expression levels, two SiHAKs were significantly decreased, and the remaining six SiHAKs had no obvious changes. Remarkably, SiHAK15 had the strongest response to K+ deficiency and high salt stress, its expression level was 151 times and 22 times of the control, respectively. (6) The differences of gene expression profiles reflected the function differences among SiHAKs from different clusters. SiHAKs from Cluster I were mainly expressed in root, implying their important roles in K+ absorption in root. SiHAKs from Cluster II generally had no tissue-specific expression characteristics, and might be involved in many biological processes, such as K+ absorption and transport, plant growth and development. SiHAKs from Cluster III were upregulated by K+ deficiency and high salt stress, inferring their potential roles in maintaining K+/Na+ balance and resisting salt stress. SiHAKs from Cluster IV were almost undetectable in gene expression in the tested tissues. SiHAKs from Cluster V had different responses to K+ deficiency and high salt stresses. Some of them were upregulated in gene expression, while others were inhibited, thus indicating that the members from Cluster V were functionally differentiated. This results not only provide the foundation for further functional studies of SiHAKs, but also provide the valuable guidance for the study of K+ efficient utilization and salt tolerance mechanism in plants.

Key words: foxtail millet, potassium transporter, KT/HAK/KUP family, salt stress, the relative expression analysis

附表1

用于SiHAK基因表达分析的引物序列信息"

基因
Gene		 引物名称
Primer name		 序列
Sequence (5°-3°)
SiHAK2 SiHAK2-F CGGCGTCCTCTCCTTCGTCT
SiHAK2-R CCCGTGGCCTTCTCTTCCTC
SiHAK3 SiHAK3-F TCTTTATTCACTGCTTTGCCG
SiHAK3-R TTCTGAGTTGGTGCCCCTCTA
SiHAK4 SiHAK4-F AAAAGTTAGCCTGCTTCCGAA
SiHAK4-R GCCGTCACCAATCACCATAGA
SiHAK6 SiHAK6-F AGGTTTCTCTTTCGTCGGGTC
SiHAK6-R TTCAAATGCTTGGGGGTTCTC
SiHAK7 SiHAK7-F ACGTGACCCTGACATAAGCAAA
SiHAK7-R TCAAGAGCCAGAGCACAACAAT
SiHAK10 SiHAK10-F CACGGAGAGCAACGAGGAGA
SiHAK10-R GCAGAGGAGGGAGTAGAGCG
SiHAK15 SiHAK15-F GAATCCCCAAATGTAAGCCG
SiHAK15-R CATGATGTATGCCACCCCAG
SiHAK16 SiHAK16-F CTCTTGCACTGGGTTGTTTTCC
SiHAK16-R GCATTTCCTATCTGGCTTTGGT
SiHAK18 SiHAK18-F ACCTTCGCTCCTGTCATCTCG
SiHAK18-R CCATCCTTCCCATTCCTTTTG
SiHAK23 SiHAK23-F CCCCCACATCTTCTCCCACT
SiHAK23-R CTTGTACCCGTACCTCGCCA
SiHAK24 SiHAK24-F GCATCCCACCCATATTCCCT
SiHAK24-R TACCCATACCGTGCCACACA
Si-actin-2 Si-actin-2-F ATCCAGCCCCTTGTATGTGA
Si-actin-2-R ACGCCCAACAATACTTGGAA

表1

谷子SiHAK基因及其蛋白质基本信息"

基因名称
Gene name		 基因序列号
Gene ID		 染色体位置
Chromosome position		 基因组大小
Genome size (bp)		 编码序列长度
Coding sequence
length (bp)		 氨基酸
Amino
acid (aa)		 分子量
Molecular
weight (kD)		 等电点 Isoelectric
point (pI)		 亚细胞定位
Subcellular location
SiHAK1 Seita.1G175000 Chr.1:25211256..25214882 forward 3627 2193 731 80.02 8.26 质膜 Plasma membrane
SiHAK2 Seita.1G307200 Chr.1:37040523..37045883 forward 5361 2322 774 86.24 7.85 质膜 Plasma membrane
SiHAK3 Seita.2G129100 Chr.2:14902256..14908174 reverse 5919 2364 788 88.61 8.49 质膜 Plasma membrane
SiHAK4 Seita.2G192700 Chr.2:28886553..28891290 reverse 4738 2568 856 94.46 7.47 质膜 Plasma membrane
SiHAK5 Seita.2G224400 Chr.2:32661560..32666230 forward 4671 2133 711 78.65 9.21 质膜 Plasma membrane
SiHAK6 Seita.2G327100 Chr.2:41466190..41473814 reverse 7625 2559 853 94.42 5.94 质膜 Plasma membrane
SiHAK7 Seita.2G427100 Chr.2:47923110..47928818 forward 5709 2352 784 87.76 8.86 质膜 Plasma membrane
SiHAK8 Seita.2G432200 Chr.2:48265283..48269697 reverse 4415 2364 788 87.21 7.61 质膜 Plasma membrane
SiHAK9 Seita.4G119700 Chr.4:12129620..12135065 reverse 5446 2331 777 85.78 8.25 质膜 Plasma membrane
SiHAK10 Seita.4G209800 Chr.4:32743375..32748151 forward 4777 2448 816 90.27 8.47 质膜 Plasma membrane
SiHAK11 Seita.4G266200 Chr.4:38390011..38398958 reverse 8948 2322 774 85.41 8.22 质膜 Plasma membrane
SiHAK12 Seita.5G168000 Chr.5:16861878..16864997 reverse 3120 2442 814 89.65 8.60 质膜 Plasma membrane
SiHAK13 Seita.5G439500 Chr.5:45554118..45559684 forward 5567 2325 775 86.47 8.52 质膜 Plasma membrane
SiHAK14 Seita.5G441200 Chr.5:45651197..45655632 reverse 4436 2205 735 80.50 8.50 质膜 Plasma membrane
SiHAK15 Seita.5G444100 Chr.5:45784733..45789729 forward 4997 2361 787 88.43 9.07 质膜 Plasma membrane
SiHAK16 Seita.6G027600 Chr.6:1995986..2001010 reverse 5025 2367 789 88.43 8.34 质膜 Plasma membrane
SiHAK17 Seita.6G205800 Chr.6:32522339..32526598 forward 4260 2220 740 82.47 8.84 质膜 Plasma membrane
SiHAK18 Seita.7G082300 Chr.7:18653291..18658866 forward 5576 2322 774 86.58 8.64 质膜 Plasma membrane
SiHAK19 Seita.7G082600 Chr.7:18675471..18680567 forward 5097 2373 791 88.54 8.82 质膜 Plasma membrane
SiHAK20 Seita.7G082700 Chr.7:18682739..18686823 forward 4085 2331 777 87.11 8.92 质膜 Plasma membrane
SiHAK21 Seita.7G082800 Chr.7:18693088..18697351 forward 4264 2286 762 85.03 6.99 质膜 Plasma membrane
SiHAK22 Seita.7G232600 Chr.7:29611687..29616556 reverse 4870 2550 850 94.73 6.15 质膜 Plasma membrane
SiHAK23 Seita.7G235500 Chr.7:29787315..29792347 reverse 5033 2412 804 89.58 8.34 质膜 Plasma membrane
SiHAK24 Seita.9G182300 Chr.9:12585631..12590025 forward 4395 2415 805 91.00 8.64 质膜 Plasma membrane
SiHAK25 Seita.9G182400 Chr.9:12603097..12608101 forward 5005 2433 811 91.93 9.02 质膜 Plasma membrane
SiHAK26 Seita.9G182500 Chr.9:12637593..12642369 forward 4777 2403 801 90.86 8.84 质膜 Plasma membrane
SiHAK27 Seita.9G182600 Chr.9:12646706..12651914 forward 5209 2415 805 90.42 8.82 质膜 Plasma membrane
SiHAK28 Seita.9G412000 Chr.9:46973981..46979758 reverse 5778 2415 805 89.58 6.82 质膜 Plasma membrane
SiHAK29 Seita.J004400 scaffold_11:162273..168095 reverse 5823 2682 894 98.77 8.68 质膜 Plasma membrane

图1

SiHAKs在谷子染色体上的分布 红色表示基因位于染色体正义链, 蓝色表示基因位于染色体反义链。"

图2

SiHAK蛋白的跨膜结构 红色的峰表示预测的跨膜螺旋。"

图3

谷子、水稻和拟南芥HAK蛋白的系统进化树"

图4

SiHAKs的基因结构和保守基序"

图5

29个SiHAKs启动子区结合的转录因子 A: 潜在结合到29个SiHAKs启动子区的转录因子家族。YABBY: YABBY结构域。WOX: WUSCHEL类同源框。TALE: 三氨基酸环延伸。GRAS: GAI、RGA和SCR。CAMTA: 钙调素结合转录激活子。C3H: 香豆酸-3-羟化酶。ARR-B: B型反应调节因子。EIL: 乙烯不敏感类。E2F/DP: E2因子/二聚体伴侣。CPP: 富含半胱氨酸的多梳样蛋白。BBR-BPC: 大麦B重组体/碱性五半胱氨酸。B3: B3结构域。LBD: 侧生组织边界结构域。HSF: 热激因子。ARF: 生长素应答因子。AP2: APETALA2。TCP: TEOSINTE BRANCHED1/ CYCLOIDEA/proliferation细胞因子。SBP: Squamosa启动子结合蛋白。MYB_related: myeloblastosis类。MIKC_MADS: MIKC型MADS (MCMI、AGAMOUS、DEFICIENS、SRF4)。bHLH: 碱性螺旋-环-螺旋。Trihelix: 三串联螺旋。GATA: GATA结合蛋白。HD-ZIP: 同源异型域-亮氨酸拉链蛋白。G2-like: Golden 2类。Dof: 单指DNA结合。bZIP: 碱性亮氨酸拉链。C2H2: Cys2/His2锌指蛋白。WRKY: WRKYGQK结构域锌指型转录因子。MYB: myeloblastosis。NAC: NAM、ATAF1/2和CUC2。ERF: 乙烯响应因子。B: 不同SiHAKs启动子上转录因子的数量。横坐标表示转录因子的数量。"

图6

SiHAKs启动子序列的转座子成分"

图7

29个SiHAKs的表达谱 A: SiHAKs在品种‘张谷’ 4个组织(根、茎、叶和穗状花序)中的表达谱。B: SiHAKs在品种豫谷1号不同组织或处理条件下的20个样品中的表达谱。a = 黑暗5 d生长出的黄花苗, b = 黑暗6 d萌发的芽, c = 2周大植株的第1片叶, d = 2周大植株的第2片叶, e = 2周大植株的第3片叶, f = 2周大植株的第4片叶, g = 2周大植株的第5片叶, h = 2周大植株的第6片叶, i = 处于stage 1的穗, j = 处于stage 2的穗穗, k = 幼根, l = 铵态氮生长条件下根, m = 干旱条件下的根, n = 硝态氮条件下的根, o = 尿素氮源条件下的根, p = 生长1周的幼茎, q = 蓝光条件下生长的幼苗, r = 黑暗条件下生长的幼苗, s = 远红光条件下生长的幼苗, t = 红光条件下生长的幼苗。"

图8

11个SiHAKs在低钾和高盐条件下根系中的表达水平 误差线表示3个独立试验的标准差。*表示显著性差异(0.01 < P < 0.05); **表示极显著差异(P < 0.01)。"

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