The pgip family in soybean and three other legume species: evidence for a birth-and-death model of evolution

Abstract

BackgroundPolygalacturonase-inhibiting proteins (PGIPs) are leucine-rich repeat (LRR) plant cell wall glycoproteins involved in plant immunity. They are typically encoded by gene families with a small number of gene copies whose evolutionary origin has been poorly investigated. Here we report the complete characterization of the full complement of the pgip family in soybean (Glycine max [L.] Merr.) and the characterization of the genomic region surrounding the pgip family in four legume species.ResultsBAC clone and genome sequence analyses showed that the soybean genome contains two pgip loci. Each locus is composed of three clustered genes that are induced following infection with the fungal pathogen Sclerotinia sclerotiorum (Lib.) de Bary, and remnant sequences of pgip genes. The analyzed homeologous soybean genomic regions (about 126 Kb) that include the pgip loci are strongly conserved and this conservation extends also to the genomes of the legume species Phaseolus vulgaris L., Medicago truncatula Gaertn. and Cicer arietinum L., each containing a single pgip locus. Maximum likelihood-based gene trees suggest that the genes within the pgip clusters have independently undergone tandem duplication in each species.ConclusionsThe paleopolyploid soybean genome contains two pgip loci comprised in large and highly conserved duplicated regions, which are also conserved in bean, M. truncatula and C. arietinum. The genomic features of these legume pgip families suggest that the forces driving the evolution of pgip genes follow the birth-and-death model, similar to that proposed for the evolution of resistance (R) genes of NBS-LRR-type.

An update on polygalacturonase-inhibiting protein (PGIP), a leucine-rich repeat protein that protects crop plants against pathogens

“…As suggested previously, these features likely have an adaptive significance for combating more efficiently a broad array of pathogens (Ferrari et al, 2003 ) or responding more rapidly to diverse environmental stimuli (D'Ovidio et al, 2004b ). In support of this view, a recent analysis of the genomic organization and composition of the legume pgip families suggested that the forces driving the evolution of the pgip genes follow the birth-and-death model (Kalunke et al, 2014 ), similarly to what proposed for the evolution of NBS-LRR-type R genes (Michelmore and Meyers, 1998 ). This possibility is based on genomic features that include inferred recent duplications, diversification as well as pseudogenization of pgip copies, as found in soybean, bean, barrel clover and chickpea (Kalunke et al, 2014 ).…”

“…In support of this view, a recent analysis of the genomic organization and composition of the legume pgip families suggested that the forces driving the evolution of the pgip genes follow the birth-and-death model (Kalunke et al, 2014 ), similarly to what proposed for the evolution of NBS-LRR-type R genes (Michelmore and Meyers, 1998 ). This possibility is based on genomic features that include inferred recent duplications, diversification as well as pseudogenization of pgip copies, as found in soybean, bean, barrel clover and chickpea (Kalunke et al, 2014 ). The organization of the pgip families therefore supports the view that tandem duplications are frequent in stress-related genes and are beneficial for survival in challenging environments (Oh et al, 2012 ).…”

“…The direction of the arrow indicates ATG to stop codon. The location of pgip genes of legume species are based on Kalunke et al ( 2014 ), those of rice and wheat on Janni et al ( 2006 ) and Di Giovanni et al ( 2008 ), and those of thale crest on Ferrari et al ( 2003 ). Chr, chromosome.…”

“…However, only a few of the more than 170 pgip genes isolated so far from different plant species have been investigated. As reported in Table 3 , individual heterologous expression and analysis of all members of a pgip family has been performed only for Arabidopsis (Ferrari et al, 2003 ), common bean (D'Ovidio et al, 2004b ), soybean (D'Ovidio et al, 2006 ; Kalunke et al, 2014 ) and wheat (Janni et al, 2013 ). PGIPs have been expressed in prokaryotic systems, as a fusion with the maltose-binding protein (MBP) (Jang et al, 2003 ; Table 3 ) or using lower temperature for bacterial growth (Chen et al, 2011 ), in Pichia pastoris and in plants by stable transformation or, transiently, by virus-mediated expression (Table 3 ).…”

Expression and validation of PvPGIP genes for resistance to white mold (Sclerotinia sclerotiorum) in common beans (Phaseolus vulgaris L.)

“…In the soybean (Glycine max), GmPGIP3, which is the most highly expressed gene of this family in the species, is phylogenetically grouped with PvPGIP1 and PvPGIP2, suggesting that the duplication that originated the ancestors of PvPGIP1/PvPGIP2 and PvPGIP3/PvPGIP4 occurred before the separation of Glycine and Phaseolus (Kalunke et al, 2014). Among these genes, PvPGIP2 is the most efficient in inhibiting the largest number of fungal PGs (Manfredini et al, 2005;D'Ovidio et al, 2004bD'Ovidio et al, , 2006.…”