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.

Felix Frimpong,Carel W Windt,Fabio Fiorani,Dagmar Van Dusschoten,Ali A Naz,Michael Frei

doi:10.3389/fpls.2021.633448

Abstract

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.

Highlights

The ability of crops to withstand Water stress (WS) is a critical aspect of the potential impact of climate change on crop productivity in agricultural systems (Ferguson, 2019; Gupta et al, 2020)
We found droughtinducible proline accumulation to be not exclusive to the leaves, rather proline significantly accumulates in barley spikes and it may contribute to the maintenance of seed initiation and grain filling (GF) processes by preventing excessive water loss
Spike proline content under WS increased by more than 30% compared with leaf proline content in all our barley genotypes

Summary

Introduction

The ability of crops to withstand WS is a critical aspect of the potential impact of climate change on crop productivity in agricultural systems (Ferguson, 2019; Gupta et al, 2020). Plants use different strategies to cope with water shortage: avoidance, escape, or tolerance. The avoidance strategy involves minimization of water loss and optimization of water uptake, which comprises physiological responses that improve photosynthetic water use efficiency, such as stomatal closure (Blum, 2005; Basu et al, 2016; Fahad et al, 2017; Rodrigues et al, 2019), stay green (Tardieu et al, 2018; Wasaya et al, 2018; Sallam et al, 2019), deeper rooting (AraiSanoh et al, 2014; Lynch and Wojciechowski, 2015; Kebede et al, 2019), or the accumulation of osmolytes and osmoprotectants (Bandurska et al, 2017). The accumulation of compatible solutes such as sugars, proline, fructans, glycine betaine, and polyamines is associated with increased drought tolerance in plants (Bhaskara et al, 2015; Templer et al, 2017; Trovato et al, 2019). Drought stress increased proline concentration about 10-fold in the leaves of monocotyledons such as rice (Oryza sativa) and dicotyledons species such as Brassica oleracea seedlings (Dien et al, 2019; Podda et al, 2019)

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