Decreased Mitochondrial Activities of Malate Dehydrogenase and Fumarase in Tomato Lead to Altered Root Growth and Architecture via Diverse Mechanisms    

Abstract

Transgenic tomato (Solanum lycopersicum) plants in which either mitochondrial malate dehydrogenase or fumarase was antisense inhibited have previously been characterized to exhibit altered photosynthetic metabolism. Here, we demonstrate that these manipulations also resulted in differences in root growth, with both transgenics being characterized by a dramatic reduction of root dry matter deposition and respiratory activity but opposite changes with respect to root area. A range of physiological, molecular, and biochemical experiments were carried out in order to determine whether changes in root morphology were due to altered metabolism within the root itself, alterations in the nature of the transformants' root exudation, consequences of alteration in the efficiency of photoassimilate delivery to the root, or a combination of these factors. Grafting experiments in which the transformants were reciprocally grafted to wild-type controls suggested that root length and area were determined by the aerial part of the plant but that biomass was not. Despite the transgenic roots displaying alteration in the expression of phytohormone-associated genes, evaluation of the levels of the hormones themselves revealed that, with the exception of gibberellins, they were largely unaltered. When taken together, these combined experiments suggest that root biomass and growth are retarded by root-specific alterations in metabolism and gibberellin contents. These data are discussed in the context of current models of root growth and biomass partitioning.

Mitochondrial Malate Dehydrogenase Lowers Leaf Respiration and Alters Photorespiration and Plant Growth in Arabidopsis

“…Work on isolated mitochondria from fruits from the same plants showed a decrease in TCA cycle flux when analyzed by NMR but no change in respiratory capacity when measured as oxygen consumption. The same workers analyzed root respiration rates and showed dramatic reductions in respiratory rate (van der Merwe et al, 2009), which is distinct from our data in Arabidopsis mutants (Fig. 4C).…”

“…This link is not absolute, however, given that short-day-grown antisense tomato plants had stunted growth, which was potentially due to impaired photosynthesis, but still had elevated levels of ascorbate due to a higher ratio of reduction of the ascorbate pool compared with the wild type (Nunes-Nesi et al, 2008). Analysis of roots from these antisense tomato plants revealed a negative impact of mMDH loss, leading to a lower root dry weight and lower root respiratory rate (van der Merwe et al, 2009). This implies a distinct impact of mMDH loss on roots and shoots.…”

Reduction of Oxalate Levels in Tomato Fruit and Consequent Metabolic Remodeling Following Overexpression of a Fungal Oxalate Decarboxylase

“…Long-distance phloem translocation of organic acids, such as malic acid, citric acid, and oxalic acid, provides a supply of metabolites before ripening; while after ripening, the metabolic pool is maintained through a feedback mechanism associated with various cellular pathways (Carrari et al, 2006;van der Merwe et al, 2009;Osorio et al, 2011). The proteomic analysis of E8.2-OXDC fruits provided insights into an effective mechanism for continual degradation of oxalic acid and maintenance of the metabolite pool, possibly through the combinatorial action of OXDC-responsive proteins.…”

Malate. Jack of all trades or master of a few?

“…Roots excrete a large number of primary and secondary compounds (Bais et al 2006;van der Merwe et al, 2009). Among the primary compounds malate is often a predominant metabolite.…”