A Wild Allele of Pyrroline-5-Carboxylate Synthase1 Leads to Proline Accumulation in Spikes and Leaves of Barley Contributing to Improved Performance Under Reduced Water Availability

Water stress (WS) during spike development strongly affects final grain yield and grain quality in cereals. Proline, an osmoprotectant amino-acid, may contribute to alleviating the effects of cell and tissue dehydration. We studied five spring barley genotypes contrasting in their drought response,...

Full description

Bibliographic Details
Main Authors: Felix Frimpong, Carel W. Windt, Dagmar van Dusschoten, Ali A. Naz, Michael Frei, Fabio Fiorani
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-02-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.633448/full
id doaj-53b99afcab9c4bfeb526f84b668665e2
record_format Article
spelling doaj-53b99afcab9c4bfeb526f84b668665e22021-02-25T06:20:18ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-02-011210.3389/fpls.2021.633448633448A Wild Allele of Pyrroline-5-Carboxylate Synthase1 Leads to Proline Accumulation in Spikes and Leaves of Barley Contributing to Improved Performance Under Reduced Water AvailabilityFelix Frimpong0Felix Frimpong1Carel W. Windt2Dagmar van Dusschoten3Ali A. Naz4Michael Frei5Fabio Fiorani6Institute of Bio- and Geosciences, IBG-2: Plant Sciences, Forschungszentrum Jülich GmbH, Jülich, GermanyCSIR-Crops Research Institute, Kumasi, GhanaInstitute of Bio- and Geosciences, IBG-2: Plant Sciences, Forschungszentrum Jülich GmbH, Jülich, GermanyInstitute of Bio- and Geosciences, IBG-2: Plant Sciences, Forschungszentrum Jülich GmbH, Jülich, GermanyDepartment of Plant Breeding, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, GermanyInstitute of Agronomy and Plant Breeding, Justus-Liebig-Universität Gießen, Gießen, GermanyInstitute of Bio- and Geosciences, IBG-2: Plant Sciences, Forschungszentrum Jülich GmbH, Jülich, GermanyWater stress (WS) during spike development strongly affects final grain yield and grain quality in cereals. Proline, an osmoprotectant amino-acid, may contribute to alleviating the effects of cell and tissue dehydration. We studied five spring barley genotypes contrasting in their drought response, including two introgression lines, S42IL-143 and S42IL-141, harboring a Pyrroline-5-carboxylate synthase1- P5cs1 allele originating from the wild barley accession ISR42-8. We tested the hypothesis that barley genotypes harboring a wild allele at P5cs1 locus are comparatively more drought-tolerant at the reproductive stage by inducing proline accumulation in their immature spikes. At the booting stage, we subjected plants to well-watered and WS treatments until physiological maturity. Several morpho-physiological traits had significant genotype by treatment interaction and reduction under WS. Varying levels of genotypic proline accumulation and differences in WS tolerance were observed. Spike proline accumulation was higher than leaf proline accumulation for all genotypes under WS. Also, introgression lines carrying a wild allele at P5cs1 locus had a markedly higher spike and leaf proline content compared with the other genotypes. These introgression lines showed milder drought symptoms compared with elite genotypes, remained photosynthetically active under WS, and maintained their intrinsic water use efficiency. These combined responses contributed to the achievement of higher final seed productivity. Magnetic resonance imaging (MRI) of whole spikes at the soft dough stage showed an increase in seed abortion among the elite genotypes compared with the introgression lines 15 days after WS treatment. Our results suggest that proline accumulation at the reproductive stage contributes to the maintenance of grain formation under water shortage.https://www.frontiersin.org/articles/10.3389/fpls.2021.633448/fullbarleyintrogression linesseed yieldproline accumulationpyrroline-5-carboxylate synthase1water stress
collection DOAJ
language English
format Article
sources DOAJ
author Felix Frimpong
Felix Frimpong
Carel W. Windt
Dagmar van Dusschoten
Ali A. Naz
Michael Frei
Fabio Fiorani
spellingShingle Felix Frimpong
Felix Frimpong
Carel W. Windt
Dagmar van Dusschoten
Ali A. Naz
Michael Frei
Fabio Fiorani
A Wild Allele of Pyrroline-5-Carboxylate Synthase1 Leads to Proline Accumulation in Spikes and Leaves of Barley Contributing to Improved Performance Under Reduced Water Availability
Frontiers in Plant Science
barley
introgression lines
seed yield
proline accumulation
pyrroline-5-carboxylate synthase1
water stress
author_facet Felix Frimpong
Felix Frimpong
Carel W. Windt
Dagmar van Dusschoten
Ali A. Naz
Michael Frei
Fabio Fiorani
author_sort Felix Frimpong
title A Wild Allele of Pyrroline-5-Carboxylate Synthase1 Leads to Proline Accumulation in Spikes and Leaves of Barley Contributing to Improved Performance Under Reduced Water Availability
title_short A Wild Allele of Pyrroline-5-Carboxylate Synthase1 Leads to Proline Accumulation in Spikes and Leaves of Barley Contributing to Improved Performance Under Reduced Water Availability
title_full A Wild Allele of Pyrroline-5-Carboxylate Synthase1 Leads to Proline Accumulation in Spikes and Leaves of Barley Contributing to Improved Performance Under Reduced Water Availability
title_fullStr A Wild Allele of Pyrroline-5-Carboxylate Synthase1 Leads to Proline Accumulation in Spikes and Leaves of Barley Contributing to Improved Performance Under Reduced Water Availability
title_full_unstemmed A Wild Allele of Pyrroline-5-Carboxylate Synthase1 Leads to Proline Accumulation in Spikes and Leaves of Barley Contributing to Improved Performance Under Reduced Water Availability
title_sort wild allele of pyrroline-5-carboxylate synthase1 leads to proline accumulation in spikes and leaves of barley contributing to improved performance under reduced water availability
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2021-02-01
description Water stress (WS) during spike development strongly affects final grain yield and grain quality in cereals. Proline, an osmoprotectant amino-acid, may contribute to alleviating the effects of cell and tissue dehydration. We studied five spring barley genotypes contrasting in their drought response, including two introgression lines, S42IL-143 and S42IL-141, harboring a Pyrroline-5-carboxylate synthase1- P5cs1 allele originating from the wild barley accession ISR42-8. We tested the hypothesis that barley genotypes harboring a wild allele at P5cs1 locus are comparatively more drought-tolerant at the reproductive stage by inducing proline accumulation in their immature spikes. At the booting stage, we subjected plants to well-watered and WS treatments until physiological maturity. Several morpho-physiological traits had significant genotype by treatment interaction and reduction under WS. Varying levels of genotypic proline accumulation and differences in WS tolerance were observed. Spike proline accumulation was higher than leaf proline accumulation for all genotypes under WS. Also, introgression lines carrying a wild allele at P5cs1 locus had a markedly higher spike and leaf proline content compared with the other genotypes. These introgression lines showed milder drought symptoms compared with elite genotypes, remained photosynthetically active under WS, and maintained their intrinsic water use efficiency. These combined responses contributed to the achievement of higher final seed productivity. Magnetic resonance imaging (MRI) of whole spikes at the soft dough stage showed an increase in seed abortion among the elite genotypes compared with the introgression lines 15 days after WS treatment. Our results suggest that proline accumulation at the reproductive stage contributes to the maintenance of grain formation under water shortage.
topic barley
introgression lines
seed yield
proline accumulation
pyrroline-5-carboxylate synthase1
water stress
url https://www.frontiersin.org/articles/10.3389/fpls.2021.633448/full
work_keys_str_mv AT felixfrimpong awildalleleofpyrroline5carboxylatesynthase1leadstoprolineaccumulationinspikesandleavesofbarleycontributingtoimprovedperformanceunderreducedwateravailability
AT felixfrimpong awildalleleofpyrroline5carboxylatesynthase1leadstoprolineaccumulationinspikesandleavesofbarleycontributingtoimprovedperformanceunderreducedwateravailability
AT carelwwindt awildalleleofpyrroline5carboxylatesynthase1leadstoprolineaccumulationinspikesandleavesofbarleycontributingtoimprovedperformanceunderreducedwateravailability
AT dagmarvandusschoten awildalleleofpyrroline5carboxylatesynthase1leadstoprolineaccumulationinspikesandleavesofbarleycontributingtoimprovedperformanceunderreducedwateravailability
AT alianaz awildalleleofpyrroline5carboxylatesynthase1leadstoprolineaccumulationinspikesandleavesofbarleycontributingtoimprovedperformanceunderreducedwateravailability
AT michaelfrei awildalleleofpyrroline5carboxylatesynthase1leadstoprolineaccumulationinspikesandleavesofbarleycontributingtoimprovedperformanceunderreducedwateravailability
AT fabiofiorani awildalleleofpyrroline5carboxylatesynthase1leadstoprolineaccumulationinspikesandleavesofbarleycontributingtoimprovedperformanceunderreducedwateravailability
AT felixfrimpong wildalleleofpyrroline5carboxylatesynthase1leadstoprolineaccumulationinspikesandleavesofbarleycontributingtoimprovedperformanceunderreducedwateravailability
AT felixfrimpong wildalleleofpyrroline5carboxylatesynthase1leadstoprolineaccumulationinspikesandleavesofbarleycontributingtoimprovedperformanceunderreducedwateravailability
AT carelwwindt wildalleleofpyrroline5carboxylatesynthase1leadstoprolineaccumulationinspikesandleavesofbarleycontributingtoimprovedperformanceunderreducedwateravailability
AT dagmarvandusschoten wildalleleofpyrroline5carboxylatesynthase1leadstoprolineaccumulationinspikesandleavesofbarleycontributingtoimprovedperformanceunderreducedwateravailability
AT alianaz wildalleleofpyrroline5carboxylatesynthase1leadstoprolineaccumulationinspikesandleavesofbarleycontributingtoimprovedperformanceunderreducedwateravailability
AT michaelfrei wildalleleofpyrroline5carboxylatesynthase1leadstoprolineaccumulationinspikesandleavesofbarleycontributingtoimprovedperformanceunderreducedwateravailability
AT fabiofiorani wildalleleofpyrroline5carboxylatesynthase1leadstoprolineaccumulationinspikesandleavesofbarleycontributingtoimprovedperformanceunderreducedwateravailability
_version_ 1724252065068220416