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. 2023 May 24;12(11):2082.
doi: 10.3390/plants12112082.

Identification of High Tolerance to Jujube Witches' Broom in Indian Jujube (Ziziphus mauritiana Lam.) and Mining Differentially Expressed Genes Related to the Tolerance through Transcriptome Analysis

Yaru Xu  1 , Chao Wang  1 , Decang Kong  2 , Ming Cao  2 , Qiong Zhang  3 , Muhammad Tahir  1 , Ying Yang  1 , Shuang Yang  1 , Wenhao Bo  1 , Xiaoming Pang  1
Affiliations

Identification of High Tolerance to Jujube Witches' Broom in Indian Jujube (Ziziphus mauritiana Lam.) and Mining Differentially Expressed Genes Related to the Tolerance through Transcriptome Analysis

Yaru Xu et al. Plants (Basel). .

Abstract

The jujube witches' broom (JWB) disease is a severe threat to jujube trees, with only a few cultivars being genuinely tolerant or resistant to phytoplasma. The defense mechanism of jujube trees against phytoplasma is still unclear. In this study, we aimed to investigate the tolerance mechanism of Indian jujube 'Cuimi' to JWB and identify the key genes that contribute to JWB high tolerance. Based on the symptoms and phytoplasma concentrations after infection, we confirmed the high tolerance of 'Cuimi' to JWB. Comparative transcriptome analysis was subsequently performed between 'Cuimi' and 'Huping', a susceptible cultivar of Chinese jujube. Unique gene ontology (GO) terms were identified in 'Cuimi', such as protein ubiquitination, cell wall biogenesis, cell surface receptor signaling pathway, oxylipin biosynthetic process, and transcription factor activity. These terms may relate to the normal development and growth of 'Cuimi' under phytoplasma infection. We identified 194 differential expressed genes related to JWB high tolerance, involved in various processes, such as reactive oxygen species (ROS), Ca2+ sensors, protein kinases, transcription factors (TFs), lignin, and hormones. Calmodulin-like (CML) genes were significantly down-regulated in infected 'Cuimi'. We speculated that the CML gene may act as a negative regulatory factor related to JWB high tolerance. Additionally, the cinnamoyl-CoA reductase-like SNL6 gene was significantly up-regulated in infected 'Cuimi', which may cause lignin deposition, limit the growth of phytoplasma, and mediate immune response of 'Cuimi' to phytoplasma. Overall, this study provides insights into the contribution of key genes to the high tolerance of JWB in Indian jujube 'Cuimi'.

Keywords: high-tolerant cultivar; jujube witches’ broom; key genes; phytoplasma concentrations.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Phenotypes and results of phytoplasma-infected ‘Cuimi’ and ‘Huping’. (A) The phenotypes of grafted ‘Cuimi’ and ‘Huping’ at 21 WAG and two healthy controls. ICM: infected ‘Cuimi’; HCM: healthy ‘Cuimi’; IHP: infected ‘Huping’; HHP: healthy ‘Huping’. (B) Detection of phytoplasma in leaves of ‘Cuimi’ and ‘Huping’ at 8 and 21 WAG. P: positive; N: negative; JS: infected ‘Jinsixiaozao’ rootstocks. (C) Phytoplasma concentrations in two cultivars. * indicates significant differences at p < 0.05; ns indicates not significant.
Figure 2
Figure 2
Screening for differentially expressed genes in ‘Cuimi’ and ‘Huping’. (A) Principal component analysis (PCA). (B) Number of DEGs in infected samples relative to healthy samples. Red indicates up-regulated DEGs; Green indicates down-regulated DEGs. (C) Venn diagram comparing DEGs in ‘Cuimi’ and ‘Huping’. (D) Sample clustering of all genes and DEGs in transcriptome analysis of ‘Cuimi’ and ‘Huping’. ICM: infected ‘Cuimi’; HCM: healthy ‘Cuimi’; IHP: infected ‘Huping’; HHP: healthy ‘Huping’.
Figure 3
Figure 3
GO classification of DEGs in jujube cultivars. DEGs in ‘Huping’ (A) and in ‘Cuimi’ (B).
Figure 4
Figure 4
GO classification of unique DEGs in jujube cultivars. Unique DEGs in ‘Huping’ (A) and in ‘Cuimi’ (B).
Figure 5
Figure 5
Pathways associated with DEGs in ‘Huping’ (A) and ‘Cuimi’ (B).
Figure 6
Figure 6
Pathway enrichment results for DEGs unique to ‘Huping’ (A) and ‘Cuimi’ (B).
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