Transcriptome-based analysis of the effects of compound microbial agents on gene expression in wheat roots and leaves under salt stress

Chao Ji; Zengwen Liang; Hui Cao; Zhizhang Chen; Xuehua Kong; Zhiwen Xin; Mingchao He; Jie Wang; Zichao Wei; Jiahao Xing; Chunyu Li; Yingxiang Zhang; Hua Zhang; Fujin Sun; Jianlin Li; Kun Li

doi:10.3389/fpls.2023.1109077

Transcriptome-based analysis of the effects of compound microbial agents on gene expression in wheat roots and leaves under salt stress

Front Plant Sci. 2023 May 10:14:1109077. doi: 10.3389/fpls.2023.1109077. eCollection 2023.

Authors

Chao Ji^{1

2

3}, Zengwen Liang^{1

2

4}, Hui Cao^{1

2}, Zhizhang Chen⁵, Xuehua Kong⁶, Zhiwen Xin^{1

2}, Mingchao He^{1

2}, Jie Wang^{1

2}, Zichao Wei^{1

2}, Jiahao Xing^{1

2}, Chunyu Li^{1

2}, Yingxiang Zhang^{1

2}, Hua Zhang^{1

2}, Fujin Sun^{1

7}, Jianlin Li^{1

8}, Kun Li^{3

9}

Affiliations

¹ College of Seed and Facility Agricultural Engineering, Weifang University, Weifang, Shandong, China.
² Key Laboratory of Biochemistry and Molecular Biology in University of Shandong Province, Weifang University, Weifang, Shandong, China.
³ Taishan Forest Ecosystem Research Station, Key Laboratory of State Forestry Administration for Silviculture of the Lower Yellow River, Shandong Agricultural University, Taian, Shandong, China.
⁴ Shandong Yongsheng Agricultural Development Co., Ltd., Yongsheng (Shouguang) Vegetable Technology Research Institute Co., Ltd, Weifang, China.
⁵ College of Foreign Languages, Weifang University, Weifang, Shandong, China.
⁶ Weifang Hanting Vestibule School, Weifang Education Bureau, Weifang, Shandong, China.
⁷ Runxin Fruit and Vegetable Cultivation Cooperative of Weifang Economic Development Zone, Weifang Agricultural Bureau, Weifang, Shandong, China.
⁸ Weifang Nuode Biotechnology Co., LTD, Weifang Agricultural Bureau, Weifang, Shandong, China.
⁹ College of Forestry, Shandong Agriculture University, Taian, Shandong, China.

Abstract

Introduction: Salt stress inhibits the beneficial effects of most plant growth-promoting rhizobacteria. The synergistic relationship between beneficial rhizosphere microorganisms and plants helps achieve more stable growth-promoting effects. This study aimed 1) to elucidate changes in gene expression profiles in the roots and leaves of wheat after inoculation with compound microbial agents and 2) to determine the mechanisms by which plant growth-promoting rhizobacteria mediate plant responses to microorganisms.

Methods: Following inoculation with compound bacteria, transcriptome characteristics of gene expression profiles of wheat, roots, and leaves at the flowering stage were investigated using Illumina high-throughput sequencing technology. Gene ontology (GO) function and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analyses were performed on the genes that were significantly differentially expressed.

Results: The expression of 231 genes in the roots of bacterial preparations (BIO) -inoculated wheat changed significantly (including 35 upregulated and 196 downregulated genes) compared with that of non-inoculated wheat. The expression of 16,321 genes in leaves changed significantly, including 9651 upregulated genes and 6670 downregulated genes. The differentially expressed genes were involved in the metabolism of carbohydrates, amino acids, and secondary compounds as well as signal transduction pathways. The ethylene receptor 1 gene in wheat leaves was significantly downregulated, and genes related to ethylene-responsive transcription factor were significantly upregulated. GO enrichment analysis showed that metabolic and cellular processes were the main functions affected in the roots and leaves. The main molecular functions altered were binding and catalytic activities, among which the cellular oxidant detoxification enrichment rate was highly expressed in the roots. The expression of peroxisome size regulation was the highest in the leaves. KEGG enrichment analysis showed that linoleic acid metabolism expression was highest in the roots, and the expression of photosynthesis-antenna proteins was the highest in leaves. After inoculation with a complex biosynthesis agent, the phenylalanine ammonia lyase (PAL) gene of the phenylpropanoid biosynthesis pathway was upregulated in wheat leaf cells while 4CL, CCR, and CYP73A were downregulated. Additionally, CYP98A and REF1 genes involved in the flavonoid biosynthesis pathway were upregulated, while F5H, HCT, CCR, E2.1.1.104, and TOGT1-related genes were downregulated.

Discussion: Differentially expressed genes may play key roles in improving salt tolerance in wheat. Compound microbial inoculants promoted the growth of wheat under salt stress and improved disease resistance by regulating the expression of metabolism-related genes in wheat roots and leaves and activating immune pathway-related genes.

Keywords: gene expression; plant growth-promoting rhizobacteria; salt stress; transcriptomic analysis; wheat.

Grants and funding

This work was supported by the National Natural Science Foundation of China (32072518), Shandong Provincial Natural Science Foundation (ZR2022QC155), Key Research and Development Project of Shandong Province (2018GNC2306), Weifang Science and Technology Development Plan Project (2022GX002), Weifang University Doctor Initiation Fund Project (208-44121013), Horizontal Topic (208-40121141).