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Acta Agronomica Sinica ›› 2023, Vol. 49 ›› Issue (9): 2385-2397.doi: 10.3724/SP.J.1006.2023.24232

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Cloning and functional analysis of sucrose transporter protein SsSWEET11 gene in sugarcane (Saccharum spontaneum L.)

DU Cui-Cui1(), WU Ming-Xing1(), ZHANG Ya-Ting1, XIE Wan-Jie1, ZHANG Ji-Sen2,*(), WANG Heng-Bo1,*()   

  1. 1Key Laboratory of Sugarcane Biology and Genetic Breeding (Fujian), Ministry of Agriculture and Rural Affairs / National Sugarcane Engineering Technology Research / College of Agriculture, Fujian Agriculture and Forestry University, Fuzhou 350002, Fujian, China
    2State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning 530004, Guangxi, China
  • Received:2022-10-16 Accepted:2023-02-10 Online:2023-09-12 Published:2023-02-21
  • About author:First author contact:**Contributed equally to this work
  • Supported by:
    National Key Research and Development Program of China(2021YFF1000104);National Undergraduate Innovation and Entrepreneurship Training Program Project(X202210389051);China Agriculture Research System of MOF and MARA(Sugar, CARS-17)

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Abstract:

SWEET (Sugars Will Eventually be Exported Transporter) proteins are widely involved in the physiological and biochemical processes of plant growth and development and response to pathogen stress by regulating the transportation, distribution, transformation, and storage of sugar in plants. This study revealed the biological function of SWEET genes in the growth and development of sugarcane and its interaction with red stripe pathogen Acidovorax avenae subsp. avenae (Aaa). Firstly, based on the PacBio full-length transcriptome cDNA library of S. spontaneum SES208 and comparative genomics, the specific primers were designed according to the re-annotated SsSWEET11 gene sequence. The full-length sequence was mined from the cDNA library by quantitative RT-PCR technology. The characteristics of the SWEET proteins were analyzed using various biological information tools, and the SWEET proteins from some plants were constructed a phylogenetic tree. Secondly, RT-qPCR detected the relative expressions of the SsSWEET11 gene with different tissues and two cultivars, ROC22 (resistant to red stripe) and MT11-610 (susceptible to red stripe). Finally, transient overexpression and subcellular localization performed the function of the SsSWEET11 gene. The results showed that the full-length cDNA sequence of the SsSWEET11 gene (GenBank accession number: OP554214) was cloned from S. spontaneum SES208, with an open reading frame of 927 bp and encoding 308 amino acid residues, which contained two MtN3_saliva domains and seven transmembrane domains. Phylogenetic analysis revealed that the SWEET protein family could be divided into four subfamilies, and SsSWEET11 belonged to subfamily III. The amino acid sequence similarity between SsSWEET11 and SbSWEET11 protein from sorghum is 97.99%. qRT-PCR demonstrated that the SsSWEET11 gene was constitutively expressed in different tissues of S. spontaneum and the relative expression level in leaves and roots was significantly higher than that in other tissues. Under the stress of Aaa, the SsSWEET11 gene presented a different expression pattern between sugarcane cultivars (ROC22) and (MT11-610) and was significantly reduced in the resistant sugarcane cultivar compared with the blank control. However, the expression of ShSWEET11 was significantly up-regulated in the susceptible sugarcane cultivar after 48 hours post-inoculation (hpi) and 72 hpi, which were 5.90 times and 5.43 times higher than the control, respectively. Subcellular localization indicated that the SsSWEET11-GFP fusion protein was located in the plasma membrane. After transiently overexpression of the SsSWEET11 gene for one day, the color of Nicotiana benthamiana leaves remained unchanged by DAB staining, and seven days after inoculation with Pseudomonas solanacearum, and Fusarium solani var. coeruleum, the incidence of transient overexpression of ShSWEET11 gene in N. benthamiana leaves were more susceptible than that of the control. Allergic reaction-related genes, jasmonic acid, and salicylic acid metabolism pathway-related genes were up-regulated, but ethylene pathway-related genes did not respond, suggesting that the SsSWEET11 gene is involved in jasmonic acid and salicylic acid signal transduction pathways, and the infection of N. benthamiana leaves by pathogens can induce an allergic reaction. These results not only provided an accumulation for the development of molecular markers associated with sugarcane resistance to Aaa but also laid a foundation for in-depth analysis of the molecular mechanism in sugarcane in response to Aaa infection.

Key words: Saccharum spontaneum, SsSWEET11 gene, sucrose transporter protein, red stripe pathogen, gene function, sugarcane

Table 1

Primers used in the study"

名称
Name		 引物序列
Primer sequences (5°-3°)		 备注
Note
CDS-SWEET11-F_27 AATCGAGCATCACCTTAGCAGTAGC 基因克隆
Gene cloning
CDS-SWEET11-R_1194 TCGTCCGAGTCGATCCGAGCC
CDS-SsSWEET11-F_72 GGAAGGAAGTCGCACTAGGAA
SsSWEET11-QF AGGTGTACCGCAAGAAGTCG 定量PCR引物
qRT-PCR primers
SsSWEET11-QR AGCGCGTAGAAGATCCACAG
GAPDH-F CACGGCCACTGGAAGCA 内参基因
Reference gene
GAPDH-R TCCTCAGGGTTCCTGATGCC
pMDC202-SsSWEET11-F CTCGACTCTAGAACTAGTATGGCAGGAGGCCTCTTCTCCAT 过表达载体构建
Construction of overexpression vector
pMDC202-SsSWEET11-R ATTTTTTCTACCGGTACCCACCGCGGCGGCGGGGAC
pSuper-1300-SsSWEET11-F GGGGCCCGGGGTCGACATGGCAGGAGGCCTCTTCTCCAT 亚细胞定位载体构建
Construction of subcellular localization vector
pSuper-1300-SsSWEET11-R CCCTTGCTCACCATGGTACCCACCGCGGCGGCGGGGAC

Fig. 1

Sequence analysis and prediction of transmembrane domain of SsSWEET11 A: the nucleic acid sequence of SsSWEET11 and its deduced amino acid sequence (The red underlined parts are the two conserved domains MtN3_saliva). B: the predicted transmembrane domain of SsSWEET11 protein."

Fig. 2

Multiple alignment of SWEET protein sequences from different species"

Fig. 3

Phylogenetic tree of SWEET family members from some species and the prediction of the conserved modifs SWEET members are from some species. AtSWEETs: Arabidopsis thaliana; OsSWEETs: Oryza sativa; SbSWEETs: Sorghum bicolor; XP_021614562.1 (MeSWEET10a): Manihot esculenta; KU686986.1 (StSWEET11) and XM_006344629.2 (StSWEET16): Solanum tuberosum; KAH9797555.1 (CsSWEET2a): Citrus sinensis; GH_D03G1971 (GhSWEET10D): Gossypium hirsutum; Medtr3g098930.1 (MtSWEET11): Medicago sativa."

Fig. 4

Relative expression pattern of SsSWEET11 genes in different tissues The error bar represents the standard error of each group treatment (n = 3). Different lowercase letters indicate significant differences at the 5% probability level."

Fig. 5

Relative expression pattern of ShSWEET11 gene in resistant and susceptible sugarcane cultivars infected by Acidovorax avenae subsp. avenae ROC22 and MT11-610 are resistant and susceptible to red stripe disease, respectively. The abscissa is the infection time of Acidovorax avenae subsp. avenae, and the ordinate is the relative expression level of SsSWEET11 gene. The error bar represents the standard error of each group treatment (n = 3). Different lowercase letters indicate significant differences at the 5% probability level."

Fig. 6

Transient expression of SsSWEET11 gene in tobacco leaves and the relative expression level of immune-related genes A-1 and B-1 represent the phenotype and DAB staining results of injection of Fusarium solani var. coeruleum and Pseudomonas solanacearum after the transient expression of the SsSWEET11 gene in tobacco leaves, respectively. Symptom 0 describes transient overexpression of the SsSWEET11 gene for 1 day, and symptoms 1 d and 7 d represent a different time when the pathogen invaded tobacco leaves after the transient overexpression of the SsSWEET11 gene. A-2 and B-2 indicate the relative expression levels of tobacco immunity-related genes after transient expression of the SsSWEET11 gene, respectively. a: the leaf phenotype after injection; b: leaves under the microscope; c: the leaf phenotype after DAB staining; d: that obtained after microscopic DAB staining. 35S::00 indicates the empty vector, and 35S::SsSWEET11 indicates the recombinant vector."

Fig. 7

Subcellular localization of SsSWEET11 protein Photographs were taken under three fields of view (visible field, green fluorescence, and merged field). 35S::GFP and 35S:: SsSWEET11::GFP were represented the results of injection of GV3101 bacterial solution with empty vector and recombinant vector into N. benthamiana leaves, respectively. Bar: 50 μm."

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