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作物学报 ›› 2025, Vol. 51 ›› Issue (5): 1230-1247.doi: 10.3724/SP.J.1006.2025.41072

• 作物遗传育种·种质资源·分子遗传学 • 上一篇    下一篇

高、低Cd积累小麦对Cd胁迫的转录组学响应差异

王青(), 王伊秀, 李越男, 吕永辉, 张海波, 刘娜*(), 程红艳*()   

  1. 山西农业大学资源环境学院, 山西太谷 030801
  • 收稿日期:2024-10-27 接受日期:2025-01-23 出版日期:2025-05-12 网络出版日期:2025-02-11
  • 通讯作者: *刘娜, E-mail: liuna@sxau.edu.cn; 程红艳, E-mail: ndchenghy@163.com
  • 作者简介:E-mail: wangqing20240805@163.com
  • 基金资助:
    国家自然科学基金项目(42107044);山西农业大学杰青优青培育工程项目(2022YQPYGC07);来晋工作奖励基金(SXBYKY2021038);山西省科技重大专项计划“揭榜挂帅”项目“特优食用菌产业关键技术研究与应用示范”(202301140601015);山西农业大学“特”“优”高质量发展科技支撑工程项目(TYGC24-03)

Differences in transcriptomic responses to cadmium stress in high/low-Cd- accumulation wheat

WANG Qing(), WANG Yi-Xiu, LI Yue-Nan, LYU Yong-Hui, ZHANG Hai-Bo, LIU Na*(), CHENG Hong-Yan*()   

  1. College of Resource and Environment, Shanxi Agricultural University, Taigu 030801, Shanxi, China
  • Received:2024-10-27 Accepted:2025-01-23 Published:2025-05-12 Published online:2025-02-11
  • Contact: *E-mail: liuna@sxau.edu.cn; E-mail: ndchenghy@163.com
  • Supported by:
    National Natural Science Foundation of China(42107044);Distinguished and Excellent Young Scholar Cultivation Project of Shanxi Agricultural University(2022YQPYGC07);Shanxi Province Excellent Doctor Award Fund(SXBYKY2021038);Shanxi Province Major Science and Technology Special Plan “Rank-Listed Project” titled “Research and Application Demonstration of Key Technologies in the Super Quality Edible Mushroom Industry”(202301140601015);Shanxi Agricultural University “Special” and “Excellent” Agricultural High Quality Development Science and Technology Support Project(TYGC24-03)

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摘要：

镉(Cd)极易被小麦吸收并对人体健康构成威胁, 且小麦响应Cd胁迫的分子机制尚不清楚。探究小麦Cd积累的分子机制对于通过遗传改良培育低Cd积累小麦至关重要。本试验采用营养液培养法, 利用转录组学测序技术研究不同Cd积累特性小麦(济麦22和周麦32)在0、0.05和0.10 mmol L-1 Cd胁迫下基因调控网络变化。京都基因与基因组百科全书(KEGG)、基因本体(GO)和蛋白-蛋白相互作用网络分析(PPI)表明, Cd胁迫诱导防御相关基因表达, 内质网蛋白质加工途径是0.05 mmol L-1 Cd胁迫下济麦22最显著富集的上调途径之一, 苯并噁嗪生物合成途径是0.10 mmol L-1 Cd胁迫下济麦22富集程度较高的上调途径之一。此外, Cd胁迫下核糖体蛋白uL13家族为PPI中主要节点, 这表明核糖体蛋白uL13家族在Cd胁迫下维持核糖体正常功能起重要作用。转运体相关基因TaNRAMP1、TaNRAMP2、TaNRAMP5、TaZIP6和TaABCG36在小麦Cd吸收和积累中起关键作用。Cd胁迫下WRKY、MYB、bHLH、bZIP转录因子表达量上调, 有助于缓解Cd胁迫造成的损伤。加权基因共表达网络和可视化分析表明, LOC123168319和LOC123145825可能是与Cd积累相关的潜在候选基因。本研究筛选出的差异基因和代谢通路, 可利用CRISPR/Cas9等基因编辑技术, 对小麦进行遗传改良, 降低其对Cd的吸收和积累能力, 为小麦抗Cd机制深入研究及后续培育低Cd积累小麦品种提供参考。

关键词: Cd胁迫, 小麦, 差异表达基因, 蛋白-蛋白相互作用, 加权基因共表达网络

Abstract:

Cadmium (Cd) is readily absorbed by wheat, posing a significant threat to human health. However, the molecular mechanisms underlying wheat’s response to Cd stress remain poorly understood. Investigating these mechanisms is essential for developing low-Cd-accumulating wheat varieties through genetic improvement. In this study, hydroponic culture combined with transcriptome sequencing was used to analyze gene regulatory network changes in two wheat varieties with differing Cd accumulation capacities (Jimai 22 and Zhoumai 32) under Cd stress at concentrations of 0, 0.05 mmol L-1, and 0.10 mmol L-1. Functional enrichment analyses using the Kyoto Encyclopedia of Genes and Genomes (KEGG), Gene Ontology (GO), and Protein-Protein Interaction (PPI) networks revealed that Cd stress induced the expression of defense-related genes. The endoplasmic reticulum protein processing pathway was the most significantly enriched upregulated pathway in Jimai 22 under 0.05 mmol L-1 Cd stress, while the benzoxazinoid biosynthesis pathway was highly enriched in Jimai 22 under 0.10 mmol L-1 Cd stress. Additionally, the ribosomal protein uL13 family was identified as a central hub in the PPI network under Cd stress, highlighting its importance in maintaining ribosomal function. Key transporters, including TaNRAMP1, TaNRAMP2, TaNRAMP5, TaZIP6, and TaABCG36, were found to play pivotal roles in Cd uptake and accumulation. Moreover, transcription factors such as WRKY, MYB, bHLH, and bZIP were upregulated under Cd stress, contributing to the alleviation of Cd-induced damage. Weighted gene co-expression network analysis (WGCNA) identified LOC123168319 and LOC123145825 as potential candidate genes associated with Cd accumulation. The differentially expressed genes and metabolic pathways identified in this study provide valuable resources for genetic improvement of wheat. Technologies such as CRISPR/Cas9 can be employed to reduce Cd absorption and accumulation, offering insights into wheat’s Cd resistance mechanisms and supporting the breeding of low-Cd wheat varieties.

Key words: Cd stress, wheat, differentially expressed gene, protein-protein interaction, weighted gene co-expression network

附表1

Cd胁迫对不同小麦品种根和地上长度和生物量的影响"

品种
Variety		 Cd浓度
Cd concentration
(mmol L-1)		 株高
Plant height
(cm)		 根长
Root length
(cm)		 地上部干重
Dry weight of the
aboveground parts (g)		 根干重
Dry weight of the roots
(g)
济麦22 Jimai 22 0 22.4 Aa 27.3 Aa 2.42 Aa 1.01 Aa
泰山24 Taishan 24 0 21.0 Aab 26.8 Aa 2.11 Aab 0.92 Aa
周麦27 Zhoumai 27 0 19.2 Ab 26.6 Aa 1.90 Ab 0.89 Aa
周麦32 Zhoumai 32 0 20.7 Aab 26.2 Aa 1.95 Ab 0.91 Aa
济麦22 Jimai 22 0.05 17.2 Ba 25.5 Aa 1.18 Ba 0.43 Ba
泰山24 Taishan 24 0.05 16.2 Ba 22.8 Bab 1.15 Bab 0.43 Bab
周麦27 Zhoumai 27 0.05 12.4 Bb 23.5 Bab 1.06 Bbc 0.41 Bab
周麦 32 Zhoumai 32 0.05 13.9 Bb 22.2 Bb 0.95 Bc 0.40 Bb
济麦22 Jimai 22 0.10 13.0 Ba 21.2 Ba 0.83 Ca 0.36 Ba
泰山24 Taishan 24 0.10 11.6 Cab 20.3 Bab 0.78 Ca 0.35 Cab
周麦27 Zhoumai 27 0.10 9.9 Cc 18.3 Cab 0.66 Cb 0.31 Cc
周麦32 Zhoumai 32 0.10 10.5 Cbc 16.9 Bb 0.63 Cb 0.32 Cbc

附图1

不同浓度Cd胁迫下不同小麦品种抗氧化酶活性 A~D分别为丙二醛(MDA)、超氧化物歧化酶(SOD)、过氧化氢酶(CAT)、过氧化物酶(POD)活性。不同小写字母表示差异显著(Tukey检验; P < 0.05)。"

附图2

不同浓度Cd胁迫下不同小麦品种巯基物质含量 A~C分别为谷胱甘肽(GSH)、非蛋白巯基(NPT)、植物螯合肽(PCs)含量。不同小写字母表示差异显著(Tukey检验; P < 0.05)。"

图1

不同浓度Cd胁迫下不同小麦品种地上部(A)和根部(B) Cd含量 不同小写字母表示同浓度不同品种间差异显著。"

图2

不同浓度 Cd 胁迫下济麦22和周麦32差异表达基因(DEG)和主成分分析(PCA)图 A: Cd胁迫下济麦22和周麦32 DEG的PCA图, Cd-22和Cd-32分别表示小麦品种济麦22和周麦32, 0、0.05和0.10分别表示Cd胁迫为 0、0.05和0.10 mmol L-1; B~D: 在CK、0.05和0.10 mmol L-1 Cd胁迫下DEG的火山图(以周麦32为对照)。X轴为基因在2个样本间的表达差异倍数, Y轴为基因表达量变化差异的统计学检验值即P值。FC表示差异表达倍数, 蓝点表示差异不显著, 绿点和红点分别表示下调和上调的基因。"

图3

不同浓度Cd胁迫下济麦22和周麦32地上部分DEG的GO和KEGG富集分析 A、B分别为CK组济麦22和周麦32 DEG的GO和KEGG富集分析; C、D分别为0.05 mmol L-1 Cd胁迫下济麦22和周麦32 DEG的GO和KEGG富集分析; E、F分别为0.10 mmol L-1 Cd胁迫下济麦22和周麦32 DEG的GO和KEGG富集分析。图中纵坐标表示pathway条目, 横坐标为注释在该条目中的DEG在注释到该条目所有DEG数的比例; 圆点的大小代表该通路中富集的DEG数, 圆点越大数目越多; 圆的颜色代表超几何检验的P值, P值越接近0, 颜色越接近红色, 富集越显著。"

图4

不同浓度Cd胁迫下Cd转运蛋白相关的DEG热图"

图5

不同浓度Cd胁迫下蛋白互作网络分析(PPI) 差异蛋白互作网络图中圆圈表示差异蛋白, 圆的颜色深度代表连接度高低, 颜色越深表示连接度越高。"

图6

不同浓度Cd胁迫下转录因子(TF)家族统计"

表1

显著性代谢通路基因统计"

通路名称
Pathway name		 基因名称
Gene name		 描述
Description		 差异表达倍数
Fold change
内质网蛋白质加工
Protein processing in the endoplasmic reticulum		 LOC123076941 16.9 kD class I heat shock protein 1-like 255.3
LOC123146971 — 144.6
LOC123065008 17.5 kD class II heat shock protein-like 115.1
LOC123145125 — 93.4
LOC123047559 — 70.1
LOC123045683 Uncharacterized LOC123045683, transcript variant X11 20.7
LOC123092591 Heat shock cognate 70 kD protein 2-like 13.9
LOC123088499 — 11.9
LOC123144151 — 8.0
LOC732706 Small heat shock protein, chloroplastic-like 7.9
苯并噁嗪生物合成
Benzoxazine
biosynthesis		 LOC123117220 — 248.9
LOC123101970 Indolin-2-one monooxygenase-like 43.6
LOC123119086 Indolin-2-one monooxygenase-like 36.4
LOC123043330 DIBOA-glucoside dioxygenase BX6-like 34.7
LOC123110087 Indolin-2-one monooxygenase-like 11.5
LOC123046742 — 9.0
LOC123150283 — 7.4
LOC123147887 — 6.2
LOC123064487 Indole-3-glycerol phosphate lyase, chloroplastic-like 2.8
LOC100682422 DIMBOA UDP-glucosyltransferase BX8 2.6
0.05 mmol L-1 Cd胁迫蛋白-蛋白相互作用
Protein-protein
interaction under
0.05 mmol L-1
Cd stress		 LOC123143519 — 2008.9
LOC123083701 — 1397.5
LOC123154376 V-type proton ATPase subunit C-like, transcript variant X3 1067.2
LOC123047031 Ubiquitin-40S ribosomal protein S27a-2-like 820.5
LOC123159281 — 316.9
LOC123137258 — 264.9
LOC123064314 60S ribosomal protein L9 113.4
LOC123068951 — 80.7
LOC123142574 Uncharacterized 53.5
LOC123039371 — 19.1
0.10 mmol L-1 Cd胁迫蛋白-蛋白相互作用
Protein-protein
interaction under
0.10 mmol L-1
Cd stress		 LOC123142574 — 1223.2
LOC123083701 — 767.6
LOC123091968 — 498.7
LOC123047031 Ubiquitin-40S ribosomal protein S27a-2-like 452.4
LOC123091201 26S proteasome non-ATPase regulatory subunit 13 homolog B-like 354.7
LOC123177030 — 277.2
LOC123129514 Glyoxysomal fatty acid beta-oxidation multifunctional protein MFP-a-like 222.8
LOC123137258 — 186.9
LOC123064314 60S ribosomal protein L9 92.4
LOC123159281 — 63.8

图7

Cd胁迫下模块与表型相关性热图 ME: 模块特征基因; A-Cd: 地上部Cd含量; R-Cd: 根部Cd含量; MDA: 丙二醛; POD: 过氧化物酶; CAT: 过氧化氢酶; SOD: 超氧化物歧化酶; GSH: 谷胱甘肽; NPT: 非蛋白巯基肽; PCs: 植物螯合肽; **为极显著差异(P < 0.01)。"

图8

Cd胁迫下与Cd相关模块KEGG富集分析和可视化分析 A, B分别为Cd胁迫下棕色、棕褐色模块的KEGG富集分析; C, D分别为浅青色模块的KEGG富集分析和可视化分析; E, F分别为暗红色模块的KEGG富集分析和可视化分析; G, H分别为蓝色模块的KEGG富集分析和可视化分析; M: 代谢; GIP: 遗传信息处理; EIP: 环境信息处理; OS: 生物体系统; CP: 细胞过程。"

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