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Acta Agronomica Sinica ›› 2022, Vol. 48 ›› Issue (4): 825-839.doi: 10.3724/SP.J.1006.2022.14080


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 Online:2022-04-12 Published:2021-08-11
  • Contact: XING Guo-Fang E-mail:jms1995mashy@163.com;sxauxgf@126.com
  • 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)


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

Table 1

Primers used in this study"

Gene name
Forward sequence (5′-3′)
Reverse sequence (5'-3')

Fig. 1

Chromosome mapping of STPs genes in foxtail millet"

Table 2

Basic physicochemical properties of STPs in foxtail millet"

Gene name
Gene ID
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

Table 3

Secondary structure prediction and subcellular localization of STPs in foxtail millet"

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
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

Fig. 2

Phylogenetic tree of STP gene family members in foxtail millet and other crops SiSTP1-SiSTP24 were members of foxtail millet STP family (red marks in the figure); SvSTP1-SvSTP26 were members of green foxtail STP family; SbSTP1-SbSTP23 were members of sorghum STP family; ZmSTP1-ZmSTP22 are members of maize STP family; TaSTP1-TaSTP33 were members of wheat STP family; OsSTP1-OsSTP27 were members of rice STP family."

Table 4

Protein motif analysis of 15 members of STPs gene family in foxtail millet"

Width (aa)
Number of genes

Fig. 3

STPs gene structure and conserved domain in foxtail millet"

Fig. 4

Prediction of cis-acting elements in promoter of STPs gene family members in foxtail millet"

Fig. 5

Collinearity analysis of STPs in Setaria italica, Oryza sativa, and Arabidopsis thaliana"

Table 5

Evolution selection pressure information of SiSTP, OsSTP, and AtSTP"

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

Fig. 6

Relative expression patterns of STPs genes in different tissues of foxtail millet Seed_30 and 60-day-after-maturation indicate seeds at 30 and 60 days after maturity, respectively. Immature-seed_S1, S2, S3, S4, S5 indicate immature seeds of S1-S5 stage, respectively. Immature-spikelet_S2, S4 indicate immature spikelet at S2 and S4 stage; Panicle_Primary- panicle-branch-differentiation-stage indicate the panicle at the initial spike branching and differentiation stages; Panicle_Third-panicle- branch-differentiation-stage indicate the panicle of the third panicle branching differentiation stage; Root_Filling-stage indicate roots at filling stage; Germinated-seeds_3-days indicates germinated seedlings for 3 days; Plant_one-tip-two-leaf indicates one tip two leaf of seedlings; Flag-leaf_filling-stage indicates flag leaf at filling stage; Leaf-top-foruth_filling-stage indicates fourth leaf at filling stage; Flag-leaf-sheath_filling-stage indicates leaf sheath at filling stage; Leaf-sheath-top-foruth_filling-stage indicates fourth parietal leaf sheath at filling stage; Leaf-top-2-3_2-days-after-heading indicates 2 and 3 top leaves two days after heading; Neck-panicle-internodes_Filling-stage indicates neck panicle-internodes at filling stage; Stem-top-second_Filling-stage indicates second section of stem at filling stage."

Fig. 7

Relative expression patterns of STPs genes under adversity stress in foxtail millet Fig. A is the relative expression analysis of low phosphorus stress, among which 0 h, 2 h, and 12 h represent the sampling time of 0, 2, and 12 hours, respectively; NP and LP represent normal phosphorus treatment and low phosphorus treatment, respectively. The Overground part and Root represent the aboveground part and Root system, respectively. Fig. B is the expression analysis of Drought stress, among which Control and Drought represent the control group and Drought treatment group, respectively. R and S represent drought-resistant and drought-sensitive varieties, respectively. M, N, and E represent different sampling time and illumination: (morning) medium illumination, (afternoon) strong illumination, and (evening) weak illumination, respectively."

Fig. 8

Relative expression patterns of STPs genes under adversity stress in foxtail millet Control and Downy mildew represent the control group and Sclerospora graminicola infection treatment group, respectively; R and S represent resistant and sensitive varieties, respectively; 3, 5, and 7 represent the 3, 5, and 7 leaf stages of different sampling time, respectively."

Fig. 9

Relative expression patterns of SiSTP4, SiSTP9, SiSTP19, and SiSTP23 genes under low phosphorus, drought, and adversity stresses in foxtail millet A: low phosphorus stress; B: drought stress; C: sclerospora graminicola infection. Abbreviations are the same as those given in Figs. 7 and 8."

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