Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (14): 2717-2731.doi: 10.3864/j.issn.0578-1752.2024.14.002

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Wheat Enolase Gene TaENO1-5B Involved in Regulating Plant Height and Grain Number Per Spike in Multiple Environments

ZHANG ZiHui1,2(), ZHANG YanFei2,3, LI Long2, LI ChaoNan2, WANG JingYi2, YANG DeLong1(), MAO XinGuo1,2(), JING RuiLian2   

  1. 1 College of Life Science and Technology, Gansu Agricultural University/State Key Laboratory of Arid Land Crop Science, Lanzhou 730070
    2 Institute of Crop Sciences, Chinese Academy of Agricultural Sciences/State Key Laboratory of Crop Gene Resources and Breeding, Beijing 100081
    3 Henan Agricultural University/National Wheat Technology Innovation Center (Preparatory), Zhengzhou 450046
  • Received:2024-01-11 Accepted:2024-02-06 Online:2024-07-24 Published:2024-07-24
  • Contact: YANG DeLong, MAO XinGuo

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Abstract:

【Objective】 Enolase is a key rate-limiting enzyme in the process of glycolysis, and plays a crucial role in plant growth and development, and response to abiotic stress. The function of common wheat enolase gene TaENO1-5B was revealed and molecular markers were developed to provide genetic resources for improving wheat through molecular breeding. 【Method】 TaENO1-5B was cloned from wheat variety Hanxuan 10. The domains of its encoded protein were analyzed on the SMART website. The secondary and tertiary structures of the protein were predicted by Phyre2 software. Real-time quantitative fluorescent PCR was used to analyze the expression levels of the target gene in wheat tissues at different developmental stages and its expression patterns under phytohormone treatment and abiotic stress. Thirty wheat germplasm with rich genetic diversity were used as plant materials to analyze the gene sequence polymorphisms, and develop molecular markers. The association analysis between TaENO1-5B haplotypes and phenotypic traits was carried out in a natural population consisting of 323 wheat accessions. The trend of breeding selection of superior haplotype in different wheat production zones in China was analyzed by using a landrace population and a modern variety population. 【Result】 TaENO1-5B gene consists of 17 exons and 16 introns encoding 446 amino acids and contains a conserved N-terminal domain and a C-terminal TIM (triose-phosphate isomerase) barrel domain. TaENO1-5B was expressed in all tissues of wheat at seedling, jointing, heading and flowering stages, and the expression level was higher in roots, root bases and spikes. The TaENO1-5B promoter region contains a variety of cis-acting elements, including elements responding to plant hormones, such as abscisic acid (ABA), auxin (IAA), and methyl jasmonate (MeJA), as well as elements responding to drought and low temperature. The expression of TaENO1-5B was significantly induced by phytohormones and abiotic stress in wheat. Four SNPs were detected in the promoter region and three SNPs in the gene region of the TaENO1-5B gene, which constituted three haplotypes, i.e., Hap-5B-1, Hap-5B-2, and Hap-5B-3. Among them, Hap-5B-2 was a favorable haplotype highly associated with shorter plant height, more spikelets per spike, and more grains per spike under various environments such as drought and high temperature, and had been positively selected in the breeding history of major wheat production zones in China. The KASP (kompetitive allele-specific PCR) marker developed based on the SNP (2 399 bp, G/A) of the TaENO1-5B promoter region was significantly correlated with the spikelet number per spike in multiple environments. 【Conclusion】 TaENO1-5B gene responds to phytohormones and abiotic stress, and is significantly correlated with plant height, spikelet number per spike and grain number per spike under various environments such as drought and high temperature. Hap-5B-2 is a favorable haplotype with shorter plant height and more number of spikelets and grains per spike. Molecular markers developed based on the variation sites of TaENO1-5B gene sequence can be used for genetic improvement of plant height and related yield traits in wheat.

Key words: wheat, TaENO1-5B, agronomic trait, KASP marker, haplotype

Table 1

Thirty wheat germplasm for testing"

序号 Number 种质 Germplasm 序号 Number 种质 Germplasm
1 沧麦6001 Cangmai 6001 16 泰山23 Taishan 23
2 冬协2号Dongxie 2 17 泰山24 Taishan 24
3 丰产1号Fengchan 1 18 太原566 Taiyuan 566
4 衡5229 Heng 5229 19 温麦6号（豫麦49）Wenmai 6 (Yumai 49)
5 葫芦头Hulutou 20 小白麦（京856）Xiaobaimai (Jing 856)
6 冀麦6号Jimai 6 21 西峰9号Xifeng 9
7 冀麦9号Jimai 9 22 西农688（西农213）Xinong 688 (Xinong 213)
8 冀麦30 Jimai 30 23 小山8号Xiaoshan 8
9 京品3号Jingpin 3 24 原冬847 Yuandong 847
10 京品11 Jingpin 11 25 运旱20410 Yunhan 20410
11 洛旱11号Luohan 11 26 运旱23-35 Yunhan 23-35
12 临旱935 Linhan 935 27 烟农21 Yannong 21
13 兰天15号Lantian 15 28 偃展一号Yanzhan 1
14 秦麦3号Qinmai 3 29 中7902 Zhong 7902
15 山农优麦2号Shannongyoumai 2 30 中作60064 Zhongzuo 60064

Table 2

Primers used in this study"

引物名称 Primer name 序列 Sequence (5′-3′)
qRT-TaENO1-5B-F AGATGACTGAAGAATGTGGAGAGC
qRT-TaENO1-5B-R GGTACATATCCGTCCCGTTCA
TaACTIN-F CTCCCTCACAACAACAACCGC
TaACTIN-R TACCAGGAACTTCCATACCAAC
TaENO1-5B-F GGAGATAGAGGCTGGGGAGG
TaENO1-5B-R AGATTTCACTACAAACTACATACGGAT
TaENO1-pro-5B-F GGGCTCCCGATTGGCTT
TaENO1-pro-5B-R TTGTGGGGACGAGGAAACTG
TaENO1-5B-SNP1-A1 GAAGGTGACCAAGTTCATGCTTCCGCCTCCTCCACCTTCATT
TaENO1-5B-SNP1-A2 GAAGGTCGGAGTCAACGGATTCCGCCTCCTCCACCTTCATC
TaENO1-5B-SNP1-C ACTCGTCGGAGCCGAGGGAG
TaENO1-5B-SNP2-A1 GAAGGTGACCAAGTTCATGCTTTTTGCCTGCTAGGAATCCGTTC
TaENO1-5B-SNP2-A2 GAAGGTCGGAGTCAACGGATTTTATTTTGCCTGCTAGGAATCCGTTT
TaENO1-5B-SNP2-C CCATCTGTGGATACACACTGTGAAAAC

Fig. 1

Analysis of TaENO1-5B gene sequence and protein structure A: Diagram of TaENO1-5B gene structure. Black rectangles indicate exons; B: Alignment of TaENO1 proteins. The red rectangular box indicates the N-terminal capped domain and the green rectangular box represents the C-terminal TIM barrel domain; C: Phylogenetic tree of TaENO1 proteins. TaENO1-5B is marked with a red dot; Ta: Triticum. aestivum; Td: Triticum dicoccoides; Hv: Hordeum vulgare; Bd: Brachypodium distachyon; Os: Oryza sativa; Pv: Panicum virgatum; Si: Setaria italica; Pm: Panicum miliaceum; Ph: Panicum halli; Zm: Zea mays; Ma: Musa acuminata subsp; At: Arabidopsis thaliana; D: Secondary structure of TaENO1-5B protein; E: Tertiary structure of TaENO1-5B protein"

Fig. 2

Expression pattern of TaENO1-5B in different tissues of wheat at different growth stages A: Seedling stage; B: Jointing stage; C: Heading stage; D: Flowering stage; R: Root; RB: Root base; L: Leaf; S: Spike; YL: Young leaf; FL: Flag leaf; US: Upper spikelet; MS: Middle spikelet; LS: Lower spikelet; P: Peduncle; PI: Peduncle internode; PN: Penultimate; PNI: Penultimate internode; AT: Antepenultimate; ATI: Antepenultimate internode; R30, R60, R90, R120, and R150 indicate the roots in 0-30 cm, 30-60 cm, 60-90 cm, 90-120 cm, and 120-150 cm soil layer, respectively; Values are the means ± SD"

Table 3

Putative cis-acting regulatory elements in the promoter region of TaENO1-5B"

顺式作用元件
Cis-acting regulatory element 		数量
Number		 生物学功能
Biological function
G-box 9 光响应元件cis-acting regulatory element involved in light responsiveness
ABRE 8 脱落酸应答元件cis-acting element involved in the abscisic acid responsiveness
TGACG-motif 3 茉莉酸甲酯应答元件cis-acting regulatory element involved in the MeJA-responsiveness
CGTCA-motif 3 茉莉酸甲酯应答元件cis-acting regulatory element involved in the MeJA-responsiveness
AuxRR-core 1 生长素应答元件cis-acting regulatory element involved in auxin responsiveness
TCA-element 1 水杨酸应答元件cis-acting element involved in salicylic acid responsiveness
MYB 2 MYB蛋白结合元件MYB protein binding element
TATA-box 29 低温胁迫应答元件cis-acting element involved in low-temperature responsiveness
DRE core 1 DREB结合元件DREB binding element

Fig. 3

Expression pattern of TaENO1-5B under different stressed treatments A: 50 µmol·L-1 abscisic acid (ABA) treatment; B: 100 μmol·L-1 auxin (IAA) treatment; C: 0.1 μmol·L-1 methyl jasmonate (MeJA) treatment; D: 16.1% (m/v) PEG treatment; E: 250 mmol·L-1 NaCl treatment; F: Low temperature (4 ℃) treatment. *, P<0.05; **, P<0.01; ***, P<0.001. The same as below"

Fig. 4

Allelic variations of TaENO1-5B and their molecular markers A: The allelic variations and haplotypes of TaENO1-5B. Black boxes indicate UTR sequences, and black rectangles represent exons; B: KASP marker KASP-SNP1 at 2 399 bp. Blue dots represent FAM-type allele A, red dots represent HEX-type allele G, and black dots are controls; C: KASP marker KASP-SNP2 at 3 864 bp. Blue dots represent FAM-type allele C, red dots represent HEX-type allele T, and black dots are controls"

Fig. 5

Association analysis between KASP-SNP1 marker and spikelet number per spike E1: 15-SY-DS-HS; E2: 15-SY-DS; E3: 15-SY-WW-HS; E4: 15-SY-WW; E5: 16-SY-DS-HS; E6: 16-SY-DS; E7: 16-SY-WW-HS; E8: 16-SY-WW; E9: 16-CP-WW; E10: 16-CP-DS; E11: 17-SY-DS-HS; E12: 17-SY-DS; E13: 17-SY-WW-HS; E14: 17-SY-WW; E15: 17-CP-WW; E16: 17-CP-DS. 15: 2015; 16: 2016; 17: 2017; SY: Shunyi; CP: Changping; WW: Well-watered; DS: Drought-stressed; HS: Heat-stressed. The same as below"

Fig. 6

Phenotypic comparisons of two TaENO1-5B haplotypes in 16 environments A: Spikelet number per spike; B: Grain number per spike; C: Spike number per plant; D: Plant height; E: Peduncle length. F: Penultimate length"

Fig. 7

Frequency distribution of TaENO1-5B haplotypes in modern varieties released in different decades in the ten wheat production zones of China A: Frequency distribution of two TaENO1-5B haplotypes in modern varieties in the ten wheat production zones of China; B: Frequency distribution of two TaENO1-5B haplotypes in modern varieties released in different decades. Ⅰ: Northern Winter Wheat Zone; Ⅱ: Yellow and Huai River Valleys Facultative Wheat Zone; Ⅲ: Middle and Low Yangtze River Valleys Autumn-Sown Spring Wheat Zone; Ⅳ: Southwestern Autumn-Sown Spring Wheat Zone; Ⅴ: Southern Autumn-Sown Spring Wheat Zone; Ⅵ: Northeastern Spring Wheat Zone; Ⅶ: Northern Spring Wheat Zone; Ⅷ: Northwestern Spring Wheat Zone; Ⅸ: Qinghai-Tibetan Plateau Spring-Winter Wheat Zone; Ⅹ: Xinjiang Winter-Spring Wheat Zone"

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