糖转运蛋白SlSWEET12c负向调控番茄对细菌性叶斑病的抗性

doi:10.16420/j.issn.0513-353x.2023-0611

摘要/Abstract

摘要：

根据番茄表达数据库（http://ted.bti.cornell.edu/cgi-bin/）及实时定量分析发现，糖转运蛋白（sugars will eventually be exported transporters）基因SlSWEET12c在番茄感病品种和抗病品种中表达差异最明显。以番茄（Solanum lycopersicum）栽培品种‘中蔬6号’为试材，获得了稳定遗传的SlSWEET12c沉默（RNAi）和过表达（OE）植株。进一步接种细菌性叶斑病病菌丁香假单胞菌（Pst DC3000）后，通过对叶片中细菌生长量、F_v/F_m变化，可溶性糖和淀粉含量、活性氧积累及防御酶活性和PR蛋白相关基因表达情况的分析，明确SWEET12c在番茄抵御Pst DC3000过程中的作用。与野生型相比，RNAi- SlSWEET12c植株接种Pst DC3000后叶片中的细菌生长量、病斑数明显减少，对Pst DC3000的抗性增强，而OE-SlSWEET12c的叶片发病更严重，细菌菌落数及褐色病斑数增多。RNAi-SlSWEET12c植株在接菌后蔗糖和淀粉含量明显高于野生型，活性氧积累少于野生型，防御酶（POD、SOD、APX）活性和PR蛋白相关基因（NPR1、PR1、PR2、PR5）表达明显升高，而OE-SlSWEET12c植株蔗糖和淀粉含量低于野生型，活性氧积累高于野生型，防御酶活性和PR蛋白相关基因表达明显低于野生型。以上结果表明SlSWEET12c通过影响叶片中糖分的组成，负向调控番茄对细菌性叶斑病的抗性。

关键词: 番茄, 糖转运蛋白, 细菌性叶斑病, SlSWEET12c

Abstract:

According to the tomato expression database（http://ted.bti.cornell.edu/cgi-bin/）and real-time quantitative analysis，the sugar transporter（sugars will eventually be exported transporter）gene SlSWEET12c showed the most obvious expression difference in tomato susceptible and resistant varieties. Using the tomato（Solanum lycopersicum）plant‘Zhongshu 6’as the test material，stable genetic SlSWEET12c silencing（RNAi）and overexpression（OE）plants were obtained. After further inoculation with Pseudomonas syringae（Pst DC3000），the role of SWEET12c in resisting Pst DC3000 in tomato was clarified through the analysis of bacterial growth，F_v/F_m change，soluble sugar and starch content，reactive oxygen species accumulation，defense enzyme activity and PR protein related gene expression in leaves. Compared with the wild type，the number of bacterial colonies and brown spots were significantly reduced in the leaves of RNAi-SlSWEET12c plants vaccinated with Pst DC3000，and the resistance to Pst DC3000 was enhanced，while OE-SlSWEET12c leaves became more severe，and the number of bacterial colonies and brown spots increased. RNAi-SlSWEET12c plants have significantly higher sucrose and starch content than wild type，reactive oxygen accumulation is less than wild type，the activity of defense enzymes （POD，SOD，APX）and PR protein related genes（NPR1，PR1，PR2，PR5）expression，while the sucrose and starch content of OE-SlSWEET12c plants is lower than wild type，reactive oxygen accumulation is higher than wild type，defense enzyme activity and PR protein related gene expression is significantly lower than wild type. The above results indicate that SlSWEET12c negatively regulates tomato resistance to bacterial leaf spot disease by affecting the composition of sugars in leaves.

Key words: tomato, sugar transporter, bacterial leaf spot disease, SlSWEET12c

邢亚男, 程杰, 刘欣, 吕书文, 吴媛媛, 姜晶. 糖转运蛋白SlSWEET12c负向调控番茄对细菌性叶斑病的抗性[J]. 园艺学报, 2024, 51(2): 321-334.

XING Yanan, CHENG Jie, LIU Xin, LÜ Shuwen, WU Yuanyuan, JIANG Jing. The Sugar Transporter SlSWEET12c Negatively Regulates Tomato Resistance to Bacterial Leaf Spot Disease[J]. Acta Horticulturae Sinica, 2024, 51(2): 321-334.

图/表 10

表1 实时荧光定量PCR引物

Table 1 The quantitative real-time PCR primers used in this experiment

基因编号 Gene accession	基因名称 Gene name	正向引物（5′-3′） Forword primer	逆向引物（5′-3′） Reverse primer
Solyc03g097580	SlSWEET10a	TGGTTGGTGGATTTGGTGC	TTGTCTCACGATGCCTAAGGG
Solyc03g097600	SlSWEET10b	TCCTTTCTCCATTGCCAACG	GCACCAAATCCACCCAC
Solyc03g097610	SlSWEET10c	GATGGCTATTGCTGGTCATTGG	ACCCTGGCTTTCTTTGGTGC
Solyc03g097870	SlSWEET11a	CTACGCACCAAAGAAAGCCAG	GTCTCACAATGCCTAAGGGAGC
Solyc03g097570	SlSWEET11b	CCAACACAACACTTCTCATCAC	GTCCACGAACAACTCCTTTG
Solyc06g072620	SlSWEET11c	GCACCAAAGAAAGCCAGGGT	CACAAGGCAAATCCATCCAAC
Solyc06g072640	SlSWEET11d	TCTCGTTCATTGTGTTCCTTGC	TGGACCTTGGCTTTCTTTGG
Solyc03g097590	SlSWEET12a	ACCAAACAAAGCCAGGGTCC	TCTCACAATGCCTAAGGGTGC
Solyc03g097620	SlSWEET12b	TGGTCTACACCTTTGGCATT	CCCTTCCGATGATTTCTTCT
Solyc05g024260	SlSWEET12c	GCATCGTGTTTCAAGTGGTTCG	TCTATCGCTGGCTTTGCGTT
Solyc06g072630	SlSWEET12d	AAGCCAGGGTCCAAACTGT	GGAATCGCAATGTTGAAGTC
Solyc03g097560	SlSWEET14	GCCAAAGGCAATCATAGAGG	AGGCACACACAATCAGACCT
Solyc09g074530	SlSWEET15	TACGCCACCAAATCGGCTAA	TGGCATGAACTCAACGCTCT
Solyc07g040690.2	SlNPR1	GGGAAAGATAGCAGCACG	GTCCACACAAACACACACATC
NC_015444.3	SlPR1	CCGTGCAATTGTGGGTGTC	GAGTTGCGCCAGACTACTTGAGT
M80604	SlPR2	TCCAGGTAGAGACAGTGGTAAA	CCTAAATATGTCGCGGTTGAGA
NM_001330783	SlPR5	TCCTTGCCTTTGTGACTT	ACCTCTTCCAGCACCATC

图1 拟南芥（At）与番茄（Sl）SWEET家族Clade Ⅲ成员氨基酸序列系统进化树

Fig. 1 Phylogenetic tree of amino acid sequence of Clade Ⅲ members of Arabidopsis（At）and SWEET family of tomato（Sl）

表2 番茄SlSWEET家族Clade Ⅲ 成员在接种细菌性叶斑病菌Pst DC3000的表达情况

Table 2 Expression of tomato SlSWEET family Clade Ⅲ members inoculated with Pst DC3000

基因名 Gene name	4 h			6 h
基因名 Gene name	抗病材料 Rio Grande-PtoR （RG-PtoR）	感病材料 Rio Grande- prf 3 （RG-prf 3）	感病材料 Rio Grande-prf 19 （RG-prf 19）	抗病材料 Rio Grande-PtoR （RG-PtoR）	感病材料 Rio Grande- prf 3 （RG-prf 3）		感病材料 Rio Grande-prf 19 （RG-prf 19）
SlSWEET10a	6.90	23.49	20.01	2.86	22.47	30.31
SlSWEET10b	8.57	8.28	9.76	8.78	21.75	25.33
SlSWEET10c	5.78	24.50	28.60	7.88	46.53	50.78
SlSWEET11a	142.08	446.79	431.44	103.71	503.59	470.25
SlSWEET11b	6.24	3.78	2.33	3.47	4.50	4.83
SlSWEET11c	0	0.77	1.87	0	4.45	5.33
SlSWEET11d	0	0	0	0	0	0.12
SlSWEET12a	13.01	67.18	60.92	4.98	67.74	74.78
SlSWEET12b	0	0	0	0	0	0
SlSWEET12c	4.99	80.27	66.06	1.22	83.32	57.78
SlSWEET12d	0.12	3.59	2.87	0.12	5.96	5.85
SlSWEET14	0.02	0.02	0	0.02	0	0
SlSWEET15	0	0	0	0	0	0

图2 ‘中蔬6号’番茄接种细菌性叶斑病菌Pst DC3000后SlSWEET家族Clade Ⅲ成员的相对表达量

Fig. 2 Relative gene expression of Clade Ⅲ members of the SlSWEET family of‘Zhongshu 6’tomato after inoculated with Pst DC3000

图3 番茄SlSWEET12c过表达（OE）和沉默（RNAi）植株基因表达水平的qRT-PCR验证 **表示与野生型（WT）差异极显著（P < 0.01）。

Fig. 3 qRT-PCR validation of gene expression levels in tomato SlSWEET12c overexpressed（OE）and silenced（RNAi）plants ** Represents an extremely significant difference from the wild-type（WT）at 0.01 level.

图4 番茄SlSWEET12c过表达（OE）和沉默（RNAi）株及野生型（WT）接种细菌性叶斑病菌Pst DC3000后的抗性表现 A：接种3 d后的表型；B：接种0 d和3 d的菌落数；C、D：接种7 d后的Fv/Fm。不同小写字母表示材料间在0.05水平差异显著。下同。

Fig. 4 Performance of resistance to tomato SlSWEET12c overexpression（OE），silencing（RNAi）lines and wild type（WT）inoculated with Pst DC3000 A：Phenotype after 3 d inoculation；B：Number of colonies at 0 d and 3 d inoculation；C，D：Fv/Fm after 7 d inoculation.Different lowercase letter indicate significant differences at 0.05 level. The same below.

图5 番茄SlSWEET12c过表达（OE）和沉默（RNAi）株接种细菌性叶斑病菌Pst DC3000后叶片可溶性糖和淀粉含量的变化

Fig. 5 Changes in soluble sugar and starch content in leaves of tomato SlSWEET12c overexpression（OE）and silence（RNAi）lines after inoculated with Pst DC3000

图6 番茄SlSWEET12c过表达（OE）和沉默（RNAi）株接种细菌性叶斑病菌Pst DC3000 3 d后过氧化氢和超氧阴离子积累 A：DAB染色观察过氧化氢积累；B：NBT染色观察超氧阴离子积累。

Fig. 6 Hydrogen peroxide accumulation and superoxide anion accumulation of tomato SlSWEET12c overexpression（OE）and silencing（RNAi）lines after inoculated with Pst DC3000 three days A：Hydrogen peroxide accumulation was observed by DAB staining；B：Superoxide anion accumulation was visualized by NBT staining.

图7 番茄SlSWEET12c过表达（OE）和沉默（RNAi）株接种细菌性叶斑病菌Pst DC3000后叶片中防御相关酶活性的变化

Fig. 7 Changes in defense-related enzyme activity in leaves of tomato SlSWEET12c overexpression（OE）and silent（RNAi）lines after inoculated with Pst DC3000

图8 番茄SlSWEET12c过表达（OE）和沉默（RNAi）株接种细菌性叶斑病菌Pst DC3000后抗病基因的表达

Fig. 8 Expression of disease resistance genes in tomato SlSWEET12c overexpression（OE）and silent（RNAi）lines after inoculated with Pst DC3000

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