Tangled history of a multigene family: The evolution of ISOPENTENYLTRANSFERASE genes.

Kanae Nishii,Yun-Yu Chen,Frank Wright,Michael Möller,Heping Cao

doi:10.1371/journal.pone.0201198

Abstract

ISOPENTENYLTRANSFERASE (IPT) genes play important roles in the initial steps of cytokinin synthesis, exist in plant and pathogenic bacteria, and form a multigene family in plants. Protein domain searches revealed that bacteria and plant IPT proteins were to assigned to different protein domains families in the Pfam database, namely Pfam IPT (IPTPfam) and Pfam IPPT (IPPTPfam) families, both are closely related in the P-loop NTPase clan. To understand the origin and evolution of the genes, a species matrix was assembled across the tree of life and intensively in plant lineages. The IPTPfam domain was only found in few bacteria lineages, whereas IPPTPfam is common except in Archaea and Mycoplasma bacteria. The bacterial IPPTPfam domain miaA genes were shown as ancestral of eukaryotic IPPTPfam domain genes. Plant IPTs diversified into class I, class II tRNA-IPTs, and Adenosine-phosphate IPTs; the class I tRNA-IPTs appeared to represent direct successors of miaA genes were found in all plant genomes, whereas class II tRNA-IPTs originated from eukaryotic genes, and were found in prasinophyte algae and in euphyllophytes. Adenosine-phosphate IPTs were only found in angiosperms. Gene duplications resulted in gene redundancies with ubiquitous expression or diversification in expression. In conclusion, it is shown that IPT genes have a complex history prior to the protein family split, and might have experienced losses or HGTs, and gene duplications that are to be likely correlated with the rise in morphological complexity involved in fine tuning cytokinin production.

Highlights

The evolution of gene families can be complex and may involve duplications within genomes or through polyploidization and loss or conversion events, these being the major forces enlarging gene families, with mutations accumulating over time further differentiating individual family members [1, 2]
We found that the cytokinin biosynthesis IPT genes in A. thaliana, AtIPT, and Oryza sativa, OsIPTs, possess an IPPTPfam domain, while these genes in A. tumefaciens, Ipt and Tzs, and Nostoc sp
The pHMM-tree analyses of the Ploop NTPase clan suggested that IPPTPfam and IPTPfam Hidden Markov Model (HMM) profiles are closely related and appear as sisters in the Neighbor Joining tree (S2 Fig)

Summary

Introduction

The evolution of gene families can be complex and may involve duplications within genomes or through polyploidization and loss or conversion events, these being the major forces enlarging gene families, with mutations accumulating over time further differentiating individual family members [1, 2]. ISOPENTENYLTRANSFERASE (IPT) enzymes regulate a rate limiting step in the biosynthesis pathway of cytokinin, an important hormone [3]. They have other functions such as stabilizing codon recognition of tRNA through the modification of tRNA in yeast. In mammals they are linked to mitochondrial diseases [4, 5]. Cytokinins are found in plants, and in plant pathogenic bacteria such as the crown-gall forming.

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Discussion

Conclusion