Hypersensitive response-like reaction is associated with hybrid necrosis in interspecific crosses between tetraploid wheat and Aegilops tauschii coss.

Nobuyuki Mizuno,Shigeo Takumi,Pyoyun Park,Naoki Hosogi,Edward Newbigin

doi:10.1371/journal.pone.0011326

Abstract

BackgroundHybrid speciation is classified into homoploid and polyploid based on ploidy level. Common wheat is an allohexaploid species that originated from a naturally occurring interploidy cross between tetraploid wheat and diploid wild wheat Aegilops tauschii Coss. Aegilops tauschii provides wide naturally occurring genetic variation. Sometimes its triploid hybrids with tetraploid wheat show the following four types of hybrid growth abnormalities: types II and III hybrid necrosis, hybrid chlorosis, and severe growth abortion. The growth abnormalities in the triploid hybrids could act as postzygotic hybridization barriers to prevent formation of hexaploid wheat.Methodology/Principal FindingsHere, we report on the geographical and phylogenetic distribution of Ae. tauschii accessions inducing the hybrid growth abnormalities and showed that they are widely distributed across growth habitats in Ae. tauschii. Molecular and cytological characterization of the type III necrosis phenotype was performed. The hybrid abnormality causing accessions were widely distributed across growth habitats in Ae. tauschii. Transcriptome analysis showed that a number of defense-related genes such as pathogenesis-related genes were highly up-regulated in the type III necrosis lines. Transmission electron microscope observation revealed that cell death occurred accompanied by generation of reactive oxygen species in leaves undergoing type III necrosis. The reduction of photosynthetic activity occurred prior to the appearance of necrotic symptoms on the leaves exhibiting hybrid necrosis.Conclusions/SignificanceTaking these results together strongly suggests that an autoimmune response might be triggered by intergenomic incompatibility between the tetraploid wheat and Ae. tauschii genomes in type III necrosis, and that genetically programmed cell death could be regarded as a hypersensitive response-like cell death similar to that observed in Arabidopsis intraspecific and Nicotiana interspecific hybrids. Only Ae. tauschii accessions without such inhibiting factors could be candidates for the D-genome donor for the present hexaploid wheat.

Highlights

Hybrid speciation is classified into two types, homoploid and polyploid, based on ploidy level [1]
The abnormal growth phenotypes are divided into four types: two types of hybrid necrosis, hybrid chlorosis, and severe growth abortion (SGA)
The number of hybrids formed from Ae. tauschii accessions and Ldn showing wild type (WT), type III necrosis, type II necrosis, hybrid chlorosis, and SGA were 61 (62.9%), 5 (5.2%), 22 (22.7%), 4 (4.1%) and 5 (5.2%), respectively (Table 1)

Summary

Introduction

Hybrid speciation is classified into two types, homoploid and polyploid, based on ploidy level [1]. The Bateson-DobzhanskyMuller (BDM) model explains the process for generating genetic incompatibilities in hybrids between two diverging lineages [2] This model proposes that reduction of fitness in hybrids generally occurs due to interaction between at least two epistatic loci derived from divergent parents. In an interspecific cross of lettuce, RIN4, which encodes a protein interacting with multiple R gene products, is one of causal genes to introduce hybrid necrosis [4]. These successful studies suggested that hybrid incompatibility might arise as a by-product of adaptive evolution [3], because the genes causing hybrid incompatibility are rapidly evolving. The growth abnormalities in the triploid hybrids could act as postzygotic hybridization barriers to prevent formation of hexaploid wheat

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