Mycorrhizal-mediated lower proline accumulation in Poncirus trifoliata under water deficit derives from the integration of inhibition of proline synthesis with increase of proline degradation.

Ying-Ning Zou,Yong-Ming Huang,Xin-Hua He,Qiang-Sheng Wu,Qiu-Dan Ni,Ji-Hong Liu

doi:10.1371/journal.pone.0080568

Abstract

Proline accumulation was often correlated with drought tolerance of plants infected by arbuscular mycorrhizal fungi (AMF), whereas lower proline in some AM plants including citrus was also found under drought stress and the relevant mechanisms have not been fully elaborated. In this study proline accumulation and activity of key enzymes relative to proline biosynthesis (▵1-pyrroline-5-carboxylate synthetase, P5CS; ornithine-δ-aminotransferase, OAT) and degradation (proline dehydrogenase, ProDH) were determined in trifoliate orange (Poncirus trifoliata, a widely used citrus rootstock) inoculated with or without Funneliformis mosseae and under well-watered (WW) or water deficit (WD). AMF colonization significantly increased plant height, stem diameter, leaf number, root volume, biomass production of both leaves and roots and leaf relative water content, irrespectively of water status. Water deficit induced more tissue proline accumulation, in company with an increase of P5CS activity, but a decrease of OAT and ProDH activity, no matter whether under AM or no-AM. Compared with no-AM treatment, AM treatment resulted in lower proline concentration and content in leaf, root, and total plant under both WW and WD. The AMF colonization significantly decreased the activity of both P5CS and OAT in leaf, root, and total plant under WW and WD, except for an insignificant difference of root OAT under WD. The AMF inoculation also generally increased tissue ProDH activity under WW and WD. Plant proline content significantly positively correlated with plant P5CS activity, negatively with plant ProDH activity, but not with plant OAT activity. These results suggest that AM plants may suffer less from WD, thereby inducing lower proline accumulation, which derives from the integration of an inhibition of proline synthesis with an enhancement of proline degradation.

Highlights

Water deficit (WD) or drought obviously limits plant growth and productivity, and plants possess a range of morphological, physiological and biochemical adaptive mechanisms in response to WD [1], [2]
The ornithine synthetic pathway, shows that proline is synthesized from ornithine in mitochondrion, which is firstly transaminated by ornithine-d-aminotransferase (OAT, EC 2.6.1.13, a key enzyme in the ornithine synthetic pathway of proline) to produce n1-pyrroline-5-carboxylate and glutamatesemialdehyde, and converted to proline [4]
OAT involves in nitrogen transformation from arginine to glutamatesemialdehyde through P5C, which is converted to glutamate by n1-pyrroline-5-carboxylate dehydrogenase [4]

Summary

Introduction

Water deficit (WD) or drought obviously limits plant growth and productivity, and plants possess a range of morphological, physiological and biochemical adaptive mechanisms in response to WD [1], [2]. Proline is synthesized mainly by the glutamate synthetic pathway in cytoplasm or chloroplast, which outlines that glutamate firstly converts into n1-pyrroline-5carboxylate by n1-pyrroline-5-carboxylate synthetase (P5CS, EC 2.7.2.11/1.2.1.41, a key enzyme in the glutamate synthetic pathway of proline) and transforms into proline by n1pyrroline-5-carboxylate reductase (P5CR) [3], [4]. The ornithine synthetic pathway, shows that proline is synthesized from ornithine in mitochondrion, which is firstly transaminated by ornithine-d-aminotransferase (OAT, EC 2.6.1.13, a key enzyme in the ornithine synthetic pathway of proline) to produce n1-pyrroline-5-carboxylate and glutamatesemialdehyde, and converted to proline [4]. The two proline synthetases, P5CS and OAT, and the proline catabolic enzyme, ProDH, are mainly involved in the net proline accumulation in plants

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