Scientia Agricultura Sinica ›› 2022, Vol. 55 ›› Issue (14): 2740-2751.doi: 10.3864/j.issn.0578-1752.2022.14.005

• PLANT PROTECTION • Previous Articles     Next Articles

Function of SlβCA3 in Plant Defense Against Pseudomonas syringae pv. tomato DC3000

FANG HanMo1(),HU ZhangJian1,MA QiaoMei1,DING ShuTing1,WANG Ping1,WANG AnRan1,SHI Kai1,2()   

  1. 1. College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058
    2. Hainan Institute of Zhejiang University, Sanya 572025, Hainan
  • Received:2021-12-23 Accepted:2022-01-25 Online:2022-07-16 Published:2022-07-26
  • Contact: Kai SHI E-mail:3150100475@zju.edu.cn;kaishi@zju.edu.cn

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Abstract:

【Background】With global climate change, the increase of atmospheric CO2 concentration is predicted to exert an influence on plant diseases, which seriously affects agricultural production. Plant β-carbonic anhydrases (βCAs) are important components in plant CO2 sensing and concentration systems and are involved in the immunity of Arabidopsis and tobacco. However, little is known about the functions of βCAs in the regulation of disease resistance in tomato (Solanum lycopersicum). 【Objective】The objective of this study is to explore the role and mechanism of tomato SlβCA3 in disease resistance, so as to provide scientific basis for resistance regulation of tomato in agricultural production. 【Method】Based on the similarity to the amino acid sequences of AtβCAs, four SlβCAs were identified in the Sol genomics network database. Wild-type (WT) tomato ‘Ailsa Craig’ (AC) was used to inoculate Pseudomonas syringae pv. tomato DC3000 (Pst DC3000) in the study. Then qRT-PCR was used to determine the transcript abundance of SlβCAs in leaves to screen the Pst DC3000-induced gene SlβCA3. Furthermore, SlβCA3 stable over-expression lines (OE-SlβCA3) were generated by Agrobacterium tumefaciens-mediated genetic transformation technology as the background of AC. OE-SlβCA3 plants were inoculated with Pst DC3000 to investigate the role of SlβCA3 in disease defense. For exploring the intrinsic mechanism of SlβCA3 regulating plant disease resistance, the transcriptome changes of WT and OE-SlβCA3 plants between inoculation with Pst DC3000 and control conditions were compared, and KEGG (Kyoto encyclopedia of genes and genomes) database was used to analyze functions of the differentially expressed genes. It is speculated that sugar metabolism pathways are involved in SlβCA3-mediated plant immunity. To verify and further analyze the conclusion, the expression of genes related to the sugar metabolism and signaling, as well as the contents of glucose, fructose and sucrose in WT and OE-SlβCA3 plants were determined. 【Result】OE-SlβCA3 plants enhanced the resistance to Pst DC3000, and showed less disease-associated cell death and a lower number of bacteria compared to the WT controls. RNA-Seq results showed that OE-SlβCA3 did not greatly change the overall transcript profile in the absence of the pathogen. In total, 2 100 Pst DC3000-induced transcripts were differentially changed in abundance. Of these, 63.3% were more abundant following Pst DC3000 inoculation in the OE-SlβCA3 plants. KEGG analysis showed that Pst DC3000-induced genes, which are dependent on SlβCA3-overexpression, were enriched in the pathways related to sugar metabolism, including starch and sucrose metabolism, protein processing in the endoplasmic reticulum (glycosylation), amino sugar and nucleotide sugar metabolism, ribosomal biosynthesis in eukaryotes and photosynthesis. Sugar metabolism is closely related to sugar signaling. Further studies found that the expression of genes related to sugar metabolism and signal transduction pathways, as well as the contents of glucose, fructose and sucrose, were higher in the leaves of OE-SlβCA3 plants than those of WT after inoculation with Pst DC3000. 【Conclusion】Overexpression of SlβCA3 in tomato enhances the resistance of plants to Pst DC3000, which may be related to the role of sugar metabolism and signaling in plant immunity.

Key words: tomato (Solanum lycopersicum), SlβCA, Pst DC3000, disease resistance, sugar metabolism, sugar signaling

Table 1

The gene-specific primers designed for qRT-PCR"

基因ID Accession number 基因Gene 正向引物Forward primer (5′-3′) 反向引物Reverse primer (5′-3′)
Solyc02g086820 SlβCA1 CAGCGAGAAAGCAGAACTTG TTTCATGTGCTCAACAGGGT
Solyc05g005490 SlβCA2 CGAGTTTGCCCATCACACAT TGCATATTCGACTGCTGCAC
Solyc02g067750 SlβCA3 AAATTGGGTTACCTGCCAAG TGGATAGGTCAGCAAGTTGG
Solyc09g010970 SlβCA4 CTTGCAGACGAACAATCACC CTCCTGGTTGAAATCCCAGT
Solyc10g083290 CWIN GAATCACAGTTGCACAGGCT GCGCATAAAGATCAGCCCAA
Solyc06g073760 BGLU AAGCCCACCTCATGCTAACT CCGCTTCACAGCATCATCAA
Solyc07g006500 TPS CTGGTACCTGCAGACACTGA AGAAGCTCTTTAGCCTGCCA
Solyc04g076810 SnRK CACAGGCGGGGAACTTTTTG ATGTTGACTCCTTCGCCAGG
Solyc01g100460 bZIP TTCCAACAGGGAATCTGCGA CTGCTCACTTCCCCTGTCAA
Solyc03g078400 SlACTIN TGGTCGGAATGGGACAGAAG CTCAGTCAGGAGAACAGGGT

Fig. 1

The phylogenetic tree construction and the expression of SlβCAs induced by Pst DC3000 inoculation"

Fig. 2

The subcellular localization of SlβCA3 Green fluorescence represents GFP signal, red fluorescence represents mCherry signal, indicating the locations of plasma membrane (A) and nucleus (B), respectively. Scale bar=50 μm"

Fig. 3

Disease symptoms in OE-SlβCA3 plants 3 d post-inoculation with Pst DC3000 A：Western blot验证OE-SlβCA3纯合过表达株系中的SlβCA3-HA融合蛋白 Detection of the SlβCA3-HA fusion protein in homozygous SlβCA3-overexpressed lines by Western blot;B：WT和OE-SlβCA3叶片接种Pst DC3000 3 d后细菌生长量 The number of bacteria in leaves on WT and OE-SlβCA3 plants 3 d post-inoculation with Pst DC3000;C：WT和OE-SlβCA3叶片接种Pst DC3000 3 d后图片 Images of leaves on WT and OE-SlβCA3 plants 3 d post-inoculation with Pst DC3000;D：WT和OE-SlβCA3叶片接种Pst DC3000 3 d后台盼蓝染色图片 Images of leaves on WT and OE-SlβCA3 plants 3 d post-inoculation with Pst DC3000 stained with trypan blue"

Fig. 4

Pathways related to SlβCA3-mediated plant immunity based on RNA-Seq analysis A：正常条件下WT和OE-SlβCA3植株全基因组转录本表达量（FPKM）散点图,纵坐标代表WT的表达丰度,横坐标代表OE-SlβCA3植株的表达丰度,红点和蓝点分别代表在WT vs OE-SlβCA3比较组中上调或下调的差异基因 Scatter plots of tomato whole-genome transcript expression (FPKM) in WT vs OE-SlβCA3 under mock-inoculated conditions. The y-axis indicates gene transcript abundance in WT, and the x-axis indicates gene transcript abundance in OE-SlβCA3. The red dots indicate up-regulated genes, while the blue dots indicate down-regulated genes in WT vs OE-SlβCA3, respectively;B：WT和OE-SlβCA3植株2100个Pst DC3000诱导基因在接种Pst DC3000与对照情况下的表达倍数热图 Heat map depicting the Pst DC3000-induced fold change in transcript levels of 2100 Pst DC3000-induced genes in WT and OE-SlβCA3 plants under mock or Pst DC3000-inoculated conditions;C：WT和OE-SlβCA3植株Pst DC3000诱导表达基因的数量韦恩图 Venn diagram showing the number of Pst DC3000-induced genes in WT and OE-SlβCA3 plants differentially;D：依赖于SlβCA3过表达的Pst DC3000诱导表达基因KEGG注释图 KEGG annotation of Pst DC3000-induced genes dependent on SlβCA3-overexpression"

Fig. 5

Effects of SlβCA3-overexpression on glucose, fructose and sucrose in tomato leaves after inoculation with Pst DC3000"

Fig. 6

The expression of genes related to sugar metabolism and signaling induced by Pst DC3000 inoculation in OE-SlβCA3 plants"

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