Expansion and evolutionary patterns of cysteine-rich peptides in plants

Abstract

Background: Cysteine-rich peptides (CRPs) are gaining recognition as regulators of cell-cell communication in plants.

Results: We identified 9556 CRPs in 12 plant species and analysed their evolutionary patterns. In most angiosperm plants, whole genome duplication and segmental duplication are the major factors driving the expansion of CRP family member genes, especially signal peptides. About 30% of the CRP genes were found clustered on the chromosomes, except in maize (Zea mays). Considerable collinearities between CRP genes between or within species reveal several syntenic regions on the chromosomes. Different subfamilies display diverse evolutionary rates, suggesting that these subfamilies are subjected to different selective pressures. CRPs in different duplication models also show contrasting evolutionary rates, although the underlying mechanism is unclear because of the complexity of gene evolution. The 1281 positively selected genes identified are probably generated within a certain period of time. While most of these belonged to maize and sorghum (Sorghum bicolor), new CRP functions would also be expected. Up-regulation of 10 CRPs was observed in self-pollinated pear pistils and pollen tubes under self S-RNase treatments in vitro. The expression divergence between different CRP gene duplication types suggests that different duplication mechanisms affected the fate of the duplicated CRPs.

Conclusion: Our analyses of the evolution of the CRP gene family provides a unique view of the evolution of this large gene family.

Keywords: Clustered genes; Cysteine-rich peptide; Divergent evolution pattern; Expression divergence; Gene duplication; Positive selection; Self-incompatibility.

Fig. 1

CRP subfamilies and their species-specific signal peptides. a Subfamily composition in all CRPs; (b) Comparison of CRPs with and without signal peptides; (c) Distribution of the different signal peptides

Fig. 2

Collinearity of CRPs in the Rosaceae. The blue lines across the chromosomes indicate collinearity between CRP gene pairs. Lines above the chromosomes indicate CRP genes. Numbers in parentheses indicate the number of collinear gene pairs. Different coloured chromosomes indicate different species: yellow, pear; maroon, peach; pink, mei and red, strawberry

Fig. 3

Comparison of CRP genes under positive selection. a CRP genes under positive selection in different subfamilies; (b) CRP genes under positive selection in different duplication types; the percentage of the corresponding total CRP genes of different duplication types are in parenthesis; (c) Number of CRP genes under positive selection by species

Fig. 4

Comparison of CRP gene Ks values. a Comparison of CRP gene Ks values in 11 angiosperm plants; (b) Comparison of Ks values between positively and negatively selected genes

Fig. 5

Comparison of evolutionary rates between CRP duplicates arising from WGD or segmental duplications and those arising from single gene duplications in pear, black cottonwood and maize; (a) pear, (b) black cottonwood, (c) maize

Fig. 6

Analysis of positively selected CRP genes in pear. a Distribution of estimated amino acid sites; (b) Maximum Likelihood phylogenetic tree constructed using three positively selected CRP genes and eight closely-related homologous genes and their corresponding conserved domains; green, three pear CRP genes; violet, recent WGD events; (c) Expression pattern of three positively selected CRP genes during pear pollen development. HP, hydrated pollen; MP, mature pollen; PT, hydrated pollen tube; SPT, stopped pollen tube

Fig. 7

Expression pattern of CRPs in self-incompatibility of pollen tubes. a Pollen tube treated with self and non-self S-RNase; (b) Pollen tube length statistics; (c) Relative expression of four CRP genes in pollen tubes with different treatments. CK (DS), normal growing ‘Dangshansuli’ pollen tubes; CK (FS), normal growing ‘Fengshui’ pollen tubes; Comp, ‘Dangshansuli’ pollen tube growth after treatment with ‘Fengshui’ S-RNase; SI, ‘Fengshui’ pollen tube growth after treatment with ‘Fengshui’ S-RNase; CK, pollen tube without S-RNase treatment