Identification and expression analysis of BURP domain-containing genes in jujube and their involvement in low temperature and drought response

Abstract

Background: Plant-specific BURP domain-containing genes are involved in plant development and stress responses. However, the role of BURP family in jujube (Ziziphus jujuba Mill.) has not been investigated.

Results: In this study, 17 BURP genes belonging to four subfamilies were identified in jujube based on homology analysis, gene structures, and conserved motif confirmation. Gene duplication analysis indicated both tandem duplication and segmental duplication had contributed to ZjBURP expansion. The ZjBURPs were extensively expressed in flowers, young fruits, and jujube leaves. Transcriptomic data and qRT-PCR analysis further revealed that ZjBURPs also significantly influence fruit development, and most genes could be induced by low temperature, salinity, and drought stresses. Notably, several BURP genes significantly altered expression in response to low temperature (ZjPG1) and drought stresses (ZjBNM7, ZjBNM8, and ZjBNM9).

Conclusions: These results provided insights into the possible roles of ZjBURPs in jujube development and stress response. These findings would help selecting candidate ZjBURP genes for cold- and drought-tolerant jujube breeding.

Keywords: Abiotic stress; BURP domain-containing protein; Fruit development; Gene expression; Ziziphus jujuba Mill.

Fig. 1

Chromosomal location and gene duplication events of ZjBURPs. The scale bar is in million bases (Mb). The genes connected with dotted gray and red lines represent the segmental (gray) and tandem (red) gene pairs, respectively

Fig. 2

The phylogenetic tree of BURP proteins and ZjBURP classification. The protein sequences from Brachypodium distachyon (10), Setaria italica (13), Oryza sativa (12), Sorghum bicolor (10), Zea mays (9), Arabidopsis thaliana (5), Glycine max (21), Cucumis sativus (6), Citrus sinensis (6), Brassica rapa (9), Populus trichocarpa (16), Vicia faba (1), and Ziziphus jujuba (17) were aligned using MUSCLE algorithm in MEGA-X, and the phylogenetic tree was constructed by MEGA-X with the neighbor-joining (NJ) method and 1,000 bootstrap replicates

Fig. 3

The phylogenetic relationships, gene structure, and conserved motifs of ZjBURPs. a The construction of the phylogenetic tree with the neighbor-joining method. b ZjBURP gene structure. c The conserved motifs identified in ZjBURP gene family

Fig. 4

Distribution of stress- and phytohormone-related cis-elements in the putative ZjBURP promoter region. The location of these cis-elements was predicted by plantCARE database

Fig. 5

ZjBURP expression in three tissues and during fruit development processes. a RT-PCR analysis of ZjBURPs in three tissues. F: flower; YF: young fruit; L: leaf. b Transcriptional abundance of ZjBURPs during fruit development of ‘Junzao’. FPKM was selected to determine ZjBURP expression levels. JYF, JE, JWM, JBR, JHR, and JFR represent the young fruit, enlargement, white maturity, beginning-red, half-red, and full- red stages of ‘Junzao,’ respectively. c Transcriptional abundance of ZjBURPs during fruit development of ‘Qingjiansuanzao’. WYF, WE, WWM, WBR, WHR, and WFR represented the young fruit, enlargement, white maturity, beginning-red, half-red, and full-red stages of ‘Qingjiansuanzao,’ respectively

Fig. 6

ZjBURP expression in low temperature. 0 h, 6 h, 12 h, 24 h, and 72 h represent the time period after the treatment. The error bars indicate the standard deviation of three biological replicates. Different letters represent a significant variation between the experimental groups (p < 0.05)

Fig. 7

ZjBURP gene expression under NaCl treatment. 0 h, 12 h, 24 h, 48 h, and 72 h represent the time period after NaCl treatment. The error bars indicate the standard deviation of three biological replicates. Different letters represent a significant variation between the experimental groups (p < 0.05)

Fig. 8

ZjBURP gene expression under PEG treatment. 0 h, 12 h, 24 h, 48 h, and 72 h represent the time period after PEG treatment. The error bars indicate the standard deviation of three biological replicates. Different letters represent a significant variation between the experimental groups (p < 0.05)