外源IAA作用下草地早熟禾中调控Cd长距离运输的关键基因表达及其代谢通路分析

doi:10.11686/cyxb2022276

摘要/Abstract

摘要：

为探究吲哚乙酸（indole-3-acetic acid， IAA）对草地早熟禾中镉（cadmium，Cd）从根系到叶片长距离运输的影响及相关机制，分析IAA作用下草地早熟禾响应Cd胁迫的差异基因及代谢通路。以草地早熟禾为试验材料，在水培条件下，叶面喷施400 nmol·L^-1外源IAA并施加600 μmol·L^-1 Cd胁迫。进行株高、根长、根系和叶片Cd含量测定及转录组测序。利用实时荧光定量验证转录组数据准确性。结果表明，外源施加IAA可促进Cd胁迫下草地早熟禾株高和根长，抑制Cd从根系向叶片的长距离运输。转录组分析发现，Cd胁迫下共有1294条基因被IAA显著调控。实时荧光定量结果与RNA-Seq表达模式一致。GO富集分析表明，IAA可调控响应高温、低温、Cd离子及病毒的相关基因抵御Cd胁迫，其中分子伴侣蛋白HSP70、激酶MAPK和转录因子MYB46被明显上调。另外，外源IAA可上调谷胱甘肽代谢及木质素合成通路上的基因，可能增加谷胱甘肽合成及细胞壁木质化，进一步增加液泡区隔化和降低Cd进入细胞，从而减少叶片Cd含量。本研究可为IAA信号作用下Cd转运与分配机制研究提供参考。

关键词: Cd胁迫, 草地早熟禾, 生长素, 转录组, Cd转运

Abstract:

This research aimed to investigate the effects and molecular mechanisms of indole-3-acetic acid （IAA）-induced decrease of the long-distance translocation of cadmium （Cd） from the roots to the shoots in Kentucky bluegrass by analysis the differentially expressed IAA-induced genes （DEGs） and metabolic pathways involved in response to Cd stress. The species Poa pratensis was used as the study material and 400 nmol·L^-1 IAA was sprayed on the leaves of plants subjected to 600 μmol·L^-1 of Cd stress. Plant heights， root lengths， and Cd concentrations in the roots and leaves were measured， and transcriptome sequencing was performed in both the Cd+ IAA and Cd treatments. Real-time quantitative polymerase chain reaction （RT-qPCR） was used to verify the accuracy of the RNA-seq. It was found that exogenous IAA significantly increased the plant heights and root lengths， and inhibited the long-distance translocation of Cd from roots to leaves. There were 1294 genes with significantly IAA-modified expression under Cd stress in Kentucky bluegrass. The expression levels of RT-qPCR had a high correlation with RNA-seq data. Gene ontology （GO） enrichment analysis showed that the genes involved in response to heat， cold， Cd， and virus exposure were induced by IAA. The molecular chaperone HSP70， protein kinase mitogen-activated protein kinase （MAPK）， and transcription factor myeloblastosis46 （MYB46） were very obviously up-regulated by IAA application. In addition， genes involved in the glutathione metabolism and lignin biosynthesis pathways were also up-regulated by exogenous IAA. This may be indicative of increased glutathione synthesis and lignification of the cell wall and further increase the vacuolar compartmentalization and decreased the Cd entry into cells， and further decrease the Cd concentration in leaves. This study provides reference data on mechanisms of IAA-induced translocation and distribution of Cd.

Key words: Cd stress, Kentucky bluegrass （Poa pratensis）, auxin, transcriptome, translocation of Cd

崔婷, 王勇, 马晖玲. 外源IAA作用下草地早熟禾中调控Cd长距离运输的关键基因表达及其代谢通路分析[J]. 草业学报, 2023, 32(6): 146-156.

Ting CUI, Yong WANG, Hui-ling MA. Analysis of the key exogenous IAA-induced gene expression levels and metabolic pathways involved in long-distance translocation of Cd in Poa pratensis[J]. Acta Prataculturae Sinica, 2023, 32(6): 146-156.

图/表 9

表1 15条随机选取的基因上下游引物序列

Table 1 Sequences of forward and reverse primer of 15 randomly selected genes

基因ID Gene ID	上游引物Forward primers	下游引物Reverse primers
TRINITY_DN115423_c2_g1	GCACATGTTCGTCGTCAAGG	AATCTCCTTCTTGTCCGGCG
TRINITY_DN145731_c0_g2	AAGAGCCATTGCCGTACTCC	TGGTCGTGCTTGGTCTCAAA
TRINITY_DN163800_c1_g2	TCTCGAGATCTGACCTGGCA	GTTCGTCGCCACTTGGAGTA
TRINITY_DN145701_c0_g1	CATCACGTCTGTGAACCCCA	GTCCGTGTTTGGGCTGTTTC
TRINITY_DN141021_c0_g2	CAACACATTCCCACCCTCCA	CAGCTGGATGTTCACCGGAT
TRINITY_DN142220_c1_g2	GACTGGCCAACTCAGACCTC	CGACCGTGACCTTCATAGGG
TRINITY_DN135644_c0_g2	TTCTACCGTTGCAGCTTCGT	TGGTGCCGTAGATGTCACAC
TRINITY_DN155113_c1_g1	CTTCACTCACTGCCAAACGC	GAGGCAAAAGACTGCTGCAC
TRINITY_DN72438_c0_g1	GACCATTGTCACCGGTCGTA	ATCTCCCTGGTTGCGGAATG
TRINITY_DN168047_c0_g1	ATCCTAGCGCCTTCATGCTC	GTACTTGCCGACACCAGTGA
TRINITY_DN139972_c1_g1	TGGCAGGCCCTACCTAGATT	TCCCAAAGCTCCTGCTTGTC
TRINITY_DN167060_c4_g1	AGGGCCGCTACTAAATACGC	CAGCACCTGAGCTTTCCTGA
TRINITY_DN163988_c1_g1	TGCAATATCCCAAGCAGCCA	CAGTCTTTAGCCCCTCACCG
TRINITY_DN165172_c2_g1	CAGCAGGCCCTGTCATTGTA	CGGTACCGGAACACGAAGAA
TRINITY_DN165077_c2_g1	CGGCGATTCTCTACCTCGTC	GCGTGGAATCGTTCTTGAGC

图1 外源IAA对Cd胁迫下草地早熟禾株高（A）、根长（B）和Cd含量（C）的影响不同小写字母和*代表不同处理间差异显著（P<0.05）。Different lowercase letters and * indicate significant differences among different treatments （P<0.05）.

Fig.1 Effects of exogenous IAA on plant height （A）， root length （B） and Cd concentration （C） in Kentucky bluegrass under Cd stress

表2 转录组测序数据结果统计

Table 2 Statistics of RNA-seq results

样本Simples	原始序列数量Raw reads	清洁序列数量Valid reads	Q₂₀ （%）	Q₃₀ （%）	GC （%）
Cd_1	47397864	46440412	98.46	94.79	52.51
Cd_2	50450066	49185876	98.54	95.08	52.75
Cd_3	51288708	50076930	98.49	94.94	52.78
Cd+IAA_1	47775358	46702260	98.51	94.97	52.66
Cd+IAA_2	52741792	51346028	98.46	94.89	52.86
Cd+IAA_3	54986698	53830218	98.53	95.05	52.72
CK_1	52312058	51101542	98.48	94.87	52.20
CK_2	44140396	43228210	98.52	94.97	52.03
CK_3	39566018	38686352	98.43	94.68	51.55
IAA_1	42275074	41366510	98.51	95.00	52.46
IAA_2	47238292	46138970	98.51	94.96	52.58
IAA_3	54196830	52731944	98.51	94.96	52.27

图2 不同处理间的差异基因数量（A）及RT-qPCR验证基因表达量（B）DEGs：差异表达基因 Differentially expressed genes.下同 The same below.

Fig.2 Number of DEGs between different treatments （A） and verification of gene expressional levels by using RT-qPCR （B）

图3 差异基因GO富集分析

Fig.3 GO enrichment analysis of DEGs

图4 Cd胁迫下外源IAA诱导的草地早熟禾对高温的响应及蛋白质磷酸化相关差异基因MIPS：磷酸肌醇合成酶Myo-inositol-1-phosphate synthase；MED37D：介导RNA聚合酶II转录Mediator of RNA polymerase II transcription subunit 37c isoform X1；DES1：鞘脂类去饱和酶4Sphingolipid delta（4）-desaturase；HSC-2：热休克蛋白同源蛋白Heat shock cognate 70 kDa protein；HSP：热休克蛋白同源蛋白Heat shock protein；UBC1：泛素缀合酶E2-16 kDa Ubiquitin-conjugating enzyme E2-16 kDa；GBLP：鸟嘌呤核苷酸结合蛋白Guanine nucleotide-binding protein subunit beta-like protein；GNB2L1：鸟嘌呤核苷酸结合蛋白Guanine nucleotide-binding protein subunit beta-like protein；Gpnmb：糖蛋白非转移性黑色素瘤蛋白B Glycoprotein non-metastatic melanoma protein B；rasG：ras相关蛋白ras-like protein；gsk：糖原合成激酶Glycogen synthase kinase；SRF1：蛋白strubbelig受体家族3-like isoform X2 Protein strubbelig-receptor family 3-like isoform X2；SLSG：G型凝集素s受体样丝氨酸/苏氨酸蛋白激酶G-type lectin S-receptor-like serine/threonine-protein kinase B120；NIK1：NSP蛋白相互作用激酶Protein NSP-interacting kinase 1-like；SD18：G型凝集素s受体样丝氨酸/苏氨酸蛋白激酶G-type lectin S-receptor-like serine/threonine-protein kinase At1g11300 At1g11301；CRLK2：富含亮氨酸重复受体样丝氨酸/苏氨酸蛋白激酶Putative leucine-rich repeat receptor-like serine/threonine-protein kinase.

Fig.4 Exogenous IAA-induced DEGs related to high temperature responding and protein phosphorylation under Cd stress

图5 Cd胁迫下外源IAA诱导的草地早熟禾对低温的响应、对Cd2+的响应、脂质代谢、信号转导、木质素生物合成及响应病毒相关差异基因ADH：乙醇脱氢酶Alcohol dehydrogenase； AHL20：核定位蛋白20-likeAT-hook motif Nuclear-localized protein 20-like AT-hook motif；CCR：肉桂酰辅酶A还原酶Cinnamoyl-CoA reductase； CIPK：钙调磷酸酶互作蛋白激酶B-LikeCalcineurin B-like-interacting protein kinase；PAG1：糖鞘脂富集微域相关磷蛋白Phosphoprotein associated with glycosphingolipid-enriched microdomains；cspLA：包含冷休克域蛋白Cold shock domain containing protein；PRX1：过氧化物酶Peroxiredoxin；TUBA：β-微管蛋白Beta-tubulin；Elovl3：长链脂肪酸延长酶Long-chain fatty acid elongase；Fabp5：脂肪酸结合蛋白Fatty acid-binding protein；Apoe：E载脂蛋白E基因Apolipoprotein；ACACA：乙酰辅酶a羧化酶1Acetyl-CoA carboxylase 1-like；ARF：ADP核基化因子ADP-ribosylation factor；Rac1：ras相关C3肉毒毒素底物Ras-related C3 botulinum toxin substrate 1-like isoform X2；ARHGDIA：鸟苷二磷酸解离抑制剂α Rho GDP （guanosine diphosphate） dissociation inhibitor α；MAPK：丝裂原激活的蛋白激酶Mitogen-activated protein kinase；fkr-3：肽基脯氨酸顺反异构酶Peptidyl-prolyl cis-trans isomerase-like；cap：环化酶Cyclase-associated 1；CYP98A1：细胞色素P450 98A1 CytochromeP450 98A1；CCR：肉桂酰辅酶A还原酶Cinnamoyl-CoA reductase；LAC4：漆酶4 Laccase4；PER52：过氧化物酶52 Peroxidase52.

Fig.5 Exogenous IAA-induced DEGs related to low temperature responding， response to Cd2+， lipid metabolism， signal transduction， lignin biosynthesis， and response to virus under Cd stress

图6 Cd胁迫下外源IAA诱导的草地早熟禾谷胱甘肽代谢过程和转录因子及转录调控相关差异基因GST：谷胱甘肽巯基转移酶Glutathione S-transferase；hpm2：谷胱甘肽巯基转移酶hmp2-like Glutathione S-transferase hmp2-like；HSP：热休克蛋白同源蛋白Heat shock protein；RAX1：类MYB98转录因子Transcription factor MYB98-like；RAP2-3：乙烯响应因子071-like isoform X2 Ethylene-responsive transcription factor ERF071-like isoform X2；CAMTA5：钙调素结合转录激活因子5 Calmodulin-binding transcription activator 5；HOX11：同源域亮氨酸拉链蛋白Homeobox-leucine zipper protein HOX11；AHL20：核定位蛋白20-like AT-hook motif Nuclear-localized protein 20-like AT-hook motif；AHL20：核定位蛋白20-like AT-hook Motif nuclear-localized protein 20；icd-1：异柠檬酸脱氢酶Isocitrate dehydrogenases；BBXL24：B-box锌指蛋白24 B-box zinc finger protein 24.

Fig.6 Exogenous IAA-induced DEGs related to glutathione metabolism， transcription factors and transcriptional regulation under Cd stress

图7 Cd胁迫下外源IAA诱导的草地早熟禾谷胱甘肽代谢及细胞壁修饰相关DEGsA：Cd胁迫下外源IAA诱导的草地早熟禾谷胱甘肽代谢相关差异基因热图；B：Cd胁迫下外源IAA诱导的草地早熟禾细胞壁修饰相关差异基因热图。A： Heatmap of exogenous IAA-induced DEGs related to glutathione metabolism in Kentucky bluegrass under Cd stress； B： Heatmap of exogenous IAA-induced DEGs related to cell wall modification in Kentucky bluegrass under Cd stress. 热图数据为经Z-score算法标准化后的基因表达量，红色代表上调，蓝色代表下调。The heatmap data was the gene expression level that normalized by Z-score method， the red color represents the up-regulated genes， while the blue color represents the down-regulated genes.

Fig.7 Exogenous IAA-induced DEGs in Kentucky bluegrass that involves in glutathione metabolism and cell wall modification under Cd stress

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