Deficiency of GDP-L-galactose phosphorylase, an enzyme required for ascorbic acid synthesis, reduces tomato fruit yield.

Matías L Alegre,Hiroshi Ezura,Charlotte Steelheart,Pierre Baldet,Daniel Just,Gustavo E Gergoff Grozeff,Carlos G Bartoli,Yoshihiro Okabe,Nicholas Smirnoff,Christophe Rothan

doi:10.1007/s00425-020-03345-x

Abstract

Reduced GDP-L-galactose phosphorylase expression and deficiency of ascorbic acid content lead to decreased fruit set and yield in tomato plants. Reduced GDP-L-galactose phosphorylase expression and deficiency of ascorbic acid content lead to decreased fruit set and yield in tomato plants. GDP-L-galactose phosphorylase (GGP) catalyzes the first step committed to ascorbic acid synthesis. The participation of GDP-L-galactose phosphorylase and ascorbate in tomato fruit production and quality was studied in this work using two SlGGP1 deficient EMS Micro-Tom mutants. The SlGGP1 mutants display decreased concentrations of ascorbate in roots, leaves, flowers, and fruit. The initiation of anthesis is delayed in ggp1 plants but the number of flowers is similar to wild type. The number of fruits is reduced in ggp1 mutants with an increased individual weight. However, the whole fruit biomass accumulation is reduced in both mutant lines. Fruits of the ggp1 plants produce more ethylene and show higher firmness and soluble solids content than the wild type after the breaker stage. Leaf CO2 uptake decreases about 50% in both ggp1 mutants at saturating light conditions; however, O2 production in an enriched CO2 atmosphere is only 19% higher in wild type leaves. Leaf conductance that is largely reduced in both mutants may be the main limitation for photosynthesis. Sink-source assays and hormone concentration were measured to determine restrictions to fruit yield. Manipulation of leaf area/fruit number relationship demonstrates that the number of fruits and not the provision of photoassimilates from the source restricts biomass accumulation in the ggp1 lines. The lower gibberellins concentration measured in the flowers would contribute to the lower fruit set, thus impacting in tomato yield. Taken as a whole these results demonstrate that ascorbate biosynthetic pathway critically participates in tomato development and fruit production.

Highlights

Ascorbate is one of the most abundant compounds in plants and there is great interest in its multiple functions as an antioxidant and enzyme cofactor (Foyer and Noctor 2011; Smirnoff 2018)
Ascorbate concentration was lower in roots and the proportion of DHA was much higher than in leaves, flowers and fruit
GDP-L-galactose phosphorylase, have ~20% of wild type ascorbate (Dowdle et al 2007; Barth et al 2010) and have small decreases in rosette leaf area and biomass, the extent most likely being sensitive to growth conditions (Lim et al 2016; Caviglia et al 2018; Plumb et al 2018)

Summary

Introduction

Ascorbate is one of the most abundant compounds in plants and there is great interest in its multiple functions as an antioxidant and enzyme cofactor (Foyer and Noctor 2011; Smirnoff 2018). It is synthesized via GDP-mannose and GDP-L-galactose and the first enzyme in this pathway considered to be specific to ascorbate synthesis is GDP-L-galactose phosphorylase (Dowdle et al 2007; Laing et al 2007, Linster et al.2007). It is encoded by paralogues in various species, including arabidopsis (VTC2 and VTC5). A range of other vtc mutants and transgenic plants in different parts of the ascorbate biosynthesis pathway with 10-20% of wild type ascorbate concentrations grow relatively normally but exhibit various subtle developmental changes, increased sensitivity to environmental stresses and increased basal resistance to pathogens (Pavet et al 2005; Barth et al 2006; Senn et al 2016; Caviglia et al 2018; Plumb et al 2018).

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