Diversity, classification and function of the plant protein kinase superfamily

Abstract

Eukaryotic protein kinases belong to a large superfamily with hundreds to thousands of copies and are components of essentially all cellular functions. The goals of this study are to classify protein kinases from 25 plant species and to assess their evolutionary history in conjunction with consideration of their molecular functions. The protein kinase superfamily has expanded in the flowering plant lineage, in part through recent duplications. As a result, the flowering plant protein kinase repertoire, or kinome, is in general significantly larger than other eukaryotes, ranging in size from 600 to 2500 members. This large variation in kinome size is mainly due to the expansion and contraction of a few families, particularly the receptor-like kinase/Pelle family. A number of protein kinases reside in highly conserved, low copy number families and often play broadly conserved regulatory roles in metabolism and cell division, although functions of plant homologues have often diverged from their metazoan counterparts. Members of expanded plant kinase families often have roles in plant-specific processes and some may have contributed to adaptive evolution. Nonetheless, non-adaptive explanations, such as kinase duplicate subfunctionalization and insufficient time for pseudogenization, may also contribute to the large number of seemingly functional protein kinases in plants.

Figure 1.

Protein kinase identification and number of protein kinases in eukaryotes. (a) Input data and analysis pipeline for identifying and classifying plant protein kinases. Model plant species: Ath, Arabidopsis thaliana; Osa, Oryza sativa; Ppa, Physcomitrella patens; Cre, Chlamydomonas reinhardtii. HMM, hidden Markov model; ML, maximum likelihood. (b) Phylogenetic relationships between and numbers of protein kinase genes in 25 plant species. Branch colour: blue, dicotyledon species; red, monocotyledon species; orange, bryophytes; green, green algae. (c) Phylogenetic relationships between selected eukaryotic species and sizes of protein kinase superfamily relative to gene numbers. Branch colour: green, Viridiplantae; blue, Apicomplexa; red, Metazoa; orange, Fungi and Microsporidia; magenta, Amoebozoa; grey, Excavata.

Figure 2.

Distributions of pairwise identities between closest protein kinase paralogues. (a) Non-plant eukaryote representatives. (b) Four model plant species with species abbreviations coloured according to the convention in figure 1b. (c) Additional dicotyledon species. (d) Additional monocotyledon species. (e) Additional bryophyte and green alga. The x-axis indicates paralogue per cent identity, and the y-axis indicates the number of paralogous pairs in an identity bin. The species abbreviations follow the species names shown in figure 1. The yellow line indicates the median paralogue identity value (also shown) for each species.

Figure 3.

Sizes of protein kinase families in 25 plant species. (a) Major groups and families. (b) RLK/Pelle subfamilies. The species abbreviations follow the species names shown in figure 1b. The number of protein kinases in each family/subfamily is colour coded according to the colour key on the lower right. Kinases that cannot be readily assigned to a group are classified as ‘plant-specific’. Within each group, some plant or algal kinases cannot be assigned to an existing family. They are designated as ‘Pl’ or ‘Cr’ for Plant and C. reinhardtii, respectively. Similarly, some kinases can be assigned to a family but not at the sub-family level. In addition to ‘Pl’ and ‘Cr’ designations, they are designated as ‘Pp’ or ‘Os’ specifying P. patens and O. sativa-specific kinases, respectively.