Polymorphism in the Chloroplast ATP Synthase Beta-Subunit Is Associated with a Maternally Inherited Enhanced Cold Recovery in Cucumber.

Madeline W Oravec,Michael J Havey

doi:10.3390/plants10061092

Madeline W Oravec, Michael J Havey

Open Access

https://doi.org/10.3390/plants10061092

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Abstract

Cucumber (Cucumis sativus L.) is a warm-season crop that is sensitive to chilling temperatures and a maternally inherited cold tolerance exists in the heirloom cultivar ‘Chipper’ (CH). Because the organelles of cucumber show differential transmission (maternal for chloroplast and paternal for mitochondrion), this cold tolerance is hypothesized to be chloroplast-associated. The goal of this research was to characterize the cold tolerant phenotype from CH and determine its genetic basis. Doubled haploid (DH) lines were produced from CH and cold susceptible cucumbers, reciprocal hybrids with identical nuclear genotypes were produced, and plants were subjected to cold treatments under lights at 4 °C for 5.5 h. Hybrid plants with CH as the maternal parent had significantly higher fresh and dry weights 14 days after cold treatment compared to the reciprocal hybrid, revealing an enhanced cold recovery phenotype maternally conferred by CH. Results from analyses of the nuclear transcriptome and reactive oxygen species (ROS) between reciprocal hybrids were consistent with the cold recovery phenotype. Sequencing of the chloroplast genome and transcriptome of the DH parents and reciprocal hybrids, respectively, revealed one maternally transmitted non-synonymous single nucleotide polymorphism (SNP) in the chloroplast F1FO-ATP synthase (CF1FO-ATPase) beta-subunit gene (atpB) of CH which confers an amino acid change from threonine to arginine. Protein modeling revealed that this change is located at the interface of the alpha- and beta-subunits in the CF1FO-ATPase complex. Polymorphisms in the CF1FO-ATPase complex have been associated with stress tolerances in other plants, and selection for or creation of polymorphic beta-subunit proteins by chloroplast transformation or gene editing could condition improved recovery from cold stress in plants.

Highlights

Cucumber (Cucumis sativus L.) is a cold-sensitive crop that can be damaged by temperatures between 1 and 12 ◦C over relatively short periods of time [1,2]
Sequencing of the chloroplast DNA (cpDNA) revealed a single nucleotide polymorphism (SNP) in the chloroplast ATPase β-Subunit Gene (atpB) of cold tolerant CH that was not present in cold susceptible Doubled haploid (DH) Straight 8’ (ST8) and MM. chloroplast RNA (cpRNA) sequencing of cold tolerant and susceptible reciprocal hybrids confirmed that the atpB SNP was maternally transmitted and maintained though transcription and RNA editing
The CH SNP results in an amino acid change in CF1 β-subunit of CF1FO-ATPase from βThr86 (ST8 and MM) to βArg86 (CH)

Summary

Introduction

Cucumber (Cucumis sativus L.) is a cold-sensitive crop that can be damaged by temperatures between 1 and 12 ◦C over relatively short periods of time [1,2]. Approaches such as spraying with hydrogen peroxide or uniconazole have been used to prepare crops for cold, but spraying is labor intensive and weather dependent [3,4]. Transgenic approaches using CBFs and other cold response genes have successfully improved cold tolerance in both chilling tolerant and sensitive species, but constitutive overexpression can confer reduced growth and productivity [19]

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