Genome-wide characterization, evolution, and expression analysis of the leucine-rich repeat receptor-like protein kinase (LRR-RLK) gene family in Rosaceae genomes

Abstract

Background: Leucine-rich repeat receptor-like protein kinase (LRR-RLK) is the largest gene family of receptor-like protein kinases (RLKs) and actively participates in regulating the growth, development, signal transduction, immunity, and stress responses of plants. However, the patterns of LRR-RLK gene family evolution in the five main Rosaceae species for which genome sequences are available have not yet been reported. In this study, we performed a comprehensive analysis of LRR-RLK genes for five Rosaceae species: Fragaria vesca (strawberry), Malus domestica (apple), Pyrus bretschneideri (Chinese white pear), Prunus mume (mei), and Prunus persica (peach), which contained 201, 244, 427, 267, and 258 LRR-RLK genes, respectively.

Results: All LRR-RLK genes were further grouped into 23 subfamilies based on the hidden Markov models approach. RLK-Pelle_LRR-XII-1, RLK-Pelle_LRR-XI-1, and RLK-Pelle_LRR-III were the three largest subfamilies. Synteny analysis indicated that there were 236 tandem duplicated genes in the five Rosaceae species, among which subfamilies XII-1 (82 genes) and XI-1 (80 genes) comprised 68.6%.

Conclusions: Our results indicate that tandem duplication made a large contribution to the expansion of the subfamilies. The gene expression, tissue-specific expression, and subcellular localization data revealed that LRR-RLK genes were differentially expressed in various organs and tissues, and the largest subfamily XI-1 was highly expressed in all five Rosaceae species, suggesting that LRR-RLKs play important roles in each stage of plant growth and development. Taken together, our results provide an overview of the LRR-RLK family in Rosaceae genomes and the basis for further functional studies.

Keywords: Gene expression; Leucine-rich repeat receptor-like protein kinase (LRR-RLK); Rosaceae; Tandem duplication.

Fig. 1

The phylogenetic tree of the species used for identifying LRR-RLK genes with whole genome duplication event marked in green star. The number in the parentheses indicate number of LRR-RLK genes in each species

Fig. 2

The phylogenetic tree for LRR-RLK genes identified in Arabidopsis and Rosaceae. A total of 1622 LRR-RLK genes were classified into 23 subfamilies and are distinguished by different colors

Fig. 3

The frequency of genes with different intron sizes in the LRR-RLK gene family in Arabidopsis, strawberry, apple, Chinese white pear, mei, and peach

Fig. 4

The circos figure for chromosome locations with segmental duplication links. a Arabidopsis thaliana, b Fragaria vesca, c Malus domestica, d Pyrus bretschneideri, e Prunus mume, f Prunus persica. The blue lines indicate segmented duplicated gene pairs that were traced to the paleohexaploidization event (~140 million years ago). The yellow lines indicate segmented duplicated gene pairs that were tranced to recent duplication event (30~45 million years ago)

Fig. 5

The heatmap of the expression of a cluster of pear genes that are highly expressed in pear pollens. The ID of the 13 genes that highly expressed in pollens are marked in red. The FPKM values are log2 transformed

Fig. 6

qRT-PCR verification of 13 pear genes in four developmental stages of pear pollens, including mature pollen grain (MP), hydrated pollen grain (HP), growing pollen tube (PT), and stopped-growth pollen tube (SPT). The Pearson Correlation Coefficient (PCC) of the expression patterns with their corresponding transcriptome data as presented in Fig. 5 are labeled for each gene

Fig. 7

Phylogenetic trees, tissue-specific expression, and subcellular localization for the pear BRI1/BRL and SERK genes. a The phylogenetic tree of the BRI1/BRL genes identified in Arabidopsis and Rosaceae. b The phylogenetic tree of the BAK1/SERK genes identified in Arabidopsis and Rosaceae. c Tissue-specific expression of pear BRI1/BRL genes. d Tissue-specific expression of pear SERK genes. e The expression of seven selected pear BRI1/BRL and SERK genes in pollen tubes before and after BR treatment. All these seven genes expression has increased after exogenous BR treatment. f Subcellular localization analysis of PbrSERK2 in the membranes of the Arabidopsis mesophyll protoplasts. YFP and FM4–64 fluorescence were localized exclusively to the membranes. Bar = 2 μm