Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (5): 855-867.doi: 10.3864/j.issn.0578-1752.2024.05.003

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

Identification of the Bru1 Genomic Region for Brown Rust Resistance and Functional Analysis of Candidate Resistance Genes in Sugarcane

WU QiBin1(), XIE WanJie1(), ZHONG Hui1, FENG ChunYan1, PAN HaoRan1, QI YiYing1, ZHANG JiSen2(), WANG HengBo1()   

  1. 1 College of Agriculture, Fujian Agriculture and Forestry University/National Engineering Research Center for Sugarcane/Key Laboratory of Sugarcane Biology and Genetic Breeding (Fujian), Ministry of Agriculture and Rural Affairs, Fuzhou 350002
    2 State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning 530004
  • Received:2023-08-28 Accepted:2023-09-25 Online:2024-03-01 Published:2024-03-06
  • Contact: ZHANG JiSen, WANG HengBo

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Abstract:

【Objective】Sugarcane brown rust, caused by Puccinia melanocephala H. Sydow & P. Sydow, is one of the most destructive fungal diseases in sugarcane industry, leading to a reduction in sucrose content by 10% to 36%. Previous studies revealed that the major gene(s) for brown rust resistance was located in the Bru1 genomic region. The cloning of crucial candidate genes and their functional investigation should provide important candidate gene resources for breeding new sugarcane cultivars resistant to brown rust.【Method】In this study, the contig-level genomic information of sugarcane cultivar ROC22 was obtained by utilizing the PacBio Sequel Ⅱ sequencing platform, and the Bru1 region associated with brown rust candidate resistance gene was identified, annotated, cloned, and analyzed for tissue specificity, expression patterns in resistant and susceptible sugarcane cultivars, subcellular localization, and transient overexpression.【Result】The results demonstrated that, firstly, using tightly associated molecular markers R12H16 and 9O20-F4 within the Bru1 region, a total of 33 genes were annotated from this region, and five candidate resistance genes (Brrg99, Brrg103, Brrg108, Brrg115, and Brrg116) were selected based on the typical/conserved domains of the resistance genes. Secondly, the full-length sequence cDNA sequence of the Brrg116 gene with an open reading frame of 729 bp and encoding 242 amino acid residues, was cloned from sugarcane cultivar ROC22. The gene sequence was aligned with the genomic databases of Saccharum spontaneum, S. officinarum, and the closely related diploid species sorghum. A high degree of sequence similarity was observed between S. spontaneum and S. officinarum, exceeding 98%. In contrast, its similarity with sorghum was 93.77%. Phylogenetic tree analysis suggests that this gene may originate from S. spontaneum species during sugarcane domestication. qRT-PCR analysis showed its constitutive expression in various tissues of sugarcane cultivars, particularly with the highest expression level in the +1 leaf, which was 5.2 times higher than in the bud. Furthermore, significantly differential expression of Brrg116 was observed at 6 h and 72 h post-inoculation with the brown rust pathogen in resistant and susceptible sugarcane cultivars. Subcellular localization analysis indicated that the encoded protein of this gene was located on the cell membrane. Finally, the Brrg116 gene was transiently overexpressed in Nicotiana benthamiana leaves, followed by inoculation with Fusarium solani var. coeruleum. The color of Nicotiana benthamiana leaves showed a gradual deepening phenotype by 3,3'-diaminobenzidine (DAB) staining. The genes related to hypersensitive response, salicylic acid, and ethylene synthesis had a sustained upregulation pattern, evidencing that the expression of these genes can enhance plant disease resistance.【Conclusion】Brrg116 was constitutively expressed in different sugarcane tissues and in response to brown rust pathogen infection, it showed a rapidly induced expression pattern in the resistant sugarcane cultivar. Overexpression of Brrg116 could trigger defense responses through hormone signaling pathways such as salicylic acid and ethylene. It is thus hypothesized that this gene may play a significant regulatory role in enhancing plant disease resistance.

Key words: sugarcane, Bru1 genomic region, brown rust disease, candidate resistance gene, diagnostic markers

Table 1

Primers used in the study"

名称
Name		 引物序列
Primer sequences (5°-3°)		 备注
Note
Brrg116-F CAAGAAATGGGCAAGAGGATG 基因克隆
Gene cloning
Brrg116-R TTGTGAATCAGCCTTGCATTT
Brrg116-QF ACCTCCCTGACTCCTTTCAT 定量PCR引物
qRT-PCR primers
Brrg116-QR CACTTAGTTGCTCCATGTCCTC
GAPDH-F CACGGCCACTGGAAGCA 甘蔗内参基因
Sugarcane reference gene
GAPDH-R TCCTCAGGGTTCCTGATGCC
NtEF-1α-F
NtEF-1α-R		 TGCTGCTGTAACAAGATGGATGC
GAGATGGGGACAAAGGGGATT		 烟草内参基因
Tobacco reference gene
pMDC202-Brrg116-F CTCGACTCTAGAACTAGTCAAGAAATGGGCAAGAGGATG 过表达载体构建
Construction of overexpression vector
pMDC202-Brrg116-R ATTTTTTCTACCGGTACCTTGTGAATCAGCCTTGCATTT
pSuper-1300-Brrg116-F GGGGCCCGGGGTCGACCAAGAAATGGGCAAGAGGATG 亚细胞定位载体构建
Construction of subcellular localization vector
pSuper-1300-Brrg116-R CCCTTGCTCACCATGGTACCTTGTGAATCAGCCTTGCATTT

Fig. 1

Comparison of Bru1 genomic sequences with BAC sequences of markers R12H16 and 9O20-F4 and prediction of candidate genes Genetic map of CG Ⅶ-1: The genome sequence of sugarcane cultivar ROC22; R12H16 and 9O20-F4: Two markers closely linked to the Bru1 locus; CIR12E3 and CIR9O20: The BAC library sequences where the markers are located. The partial content of the figure is from research reports by COSTET, et al[6]"

Fig. 2

Multiple sequence alignment and phylogenetic analysis of multiple alleles of Brrg116 A: Displayed the representative orthologous gene sequences of S. spontaneum, S. officinarum, sugarcane cultivar, and sorghum; B: Showed the phylogenetic tree of Brrg116 multiple alleles. Pink indicated the multiple alleles from S. spontaneum. Light blue indicated the multiple alleles from S. spontaneum. Green indicated the multiple alleles from the closely related Sorghum bicolor"

Fig. 3

Tissue-specific expression of Brrg116 gene in sugarcane"

Fig. 4

The relative expression pattern of Brrg116 genes under brown rust infection ROC22 and YT60 are brown rust resistant and susceptible sugarcane cultivars, respectively"

Fig. 5

Subcellular localization of Brrg116 protein pSuper1300-35S::GFP and pSuper1300-35S::Brrg116::GFP vectors were represented empty and recombinant plasmids, respectively. Bar scale =50 µm"

Fig. 6

The symptom of Nicotiana benthamiana disease and the content of H2O2 and the expression of immune-related genes A and B represented the phenotype and DAB staining results of tobacco leaves inoculated with Fusarium solani var. coeruleum after Brrg116 gene transiently overexpressed in tobacco leaves. Symptom 1 d, 3 d and 7 d indicated the time of inoculation of Fusarium solani var. coeruleum after transient overexpression of the Brrg116 gene, respectively. C: The expression levels of genes related to tobacco hypersensitivity response and SA and ethylene synthesis after overexpression of Brrg116 gene. Different lowercase letters indicate significant differences at the P<0.05 probability level"

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