Metabolic and enzymatic changes associated with carbon mobilization, utilization and replenishment triggered in grain amaranth (Amaranthus cruentus) in response to partial defoliation by mechanical injury or insect herbivory

Abstract

BackgroundAmaranthus cruentus and A. hypochondriacus are crop plants grown for grain production in subtropical countries. Recently, the generation of large-scale transcriptomic data opened the possibility to study representative genes of primary metabolism to gain a better understanding of the biochemical mechanisms underlying tolerance to defoliation in these species. A multi-level approach was followed involving gene expression analysis, enzyme activity and metabolite measurements.ResultsDefoliation by insect herbivory (HD) or mechanical damage (MD) led to a rapid and transient reduction of non-structural carbohydrates (NSC) in all tissues examined. This correlated with a short-term induction of foliar sucrolytic activity, differential gene expression of a vacuolar invertase and its inhibitor, and induction of a sucrose transporter gene. Leaf starch in defoliated plants correlated negatively with amylolytic activity and expression of a β-amylase-1 gene and positively with a soluble starch synthase gene. Fatty-acid accumulation in roots coincided with a high expression of a phosphoenolpyruvate/phosphate transporter gene. In all tissues there was a long-term replenishment of most metabolite pools, which allowed damaged plants to maintain unaltered growth and grain yield. Promoter analysis of ADP-glucose pyrophosphorylase and vacuolar invertase genes indicated the presence of cis-regulatory elements that supported their responsiveness to defoliation. HD and MD had differential effects on transcripts, enzyme activities and metabolites. However, the correlation between transcript abundance and enzymatic activities was very limited. A better correlation was found between enzymes, metabolite levels and growth and reproductive parameters.ConclusionsIt is concluded that a rapid reduction of NSC reserves in leaves, stems and roots followed by their long-term recovery underlies tolerance to defoliation in grain amaranth. This requires the coordinate action of genes/enzymes that are differentially affected by the way leaf damage is performed. Defoliation tolerance in grain is a complex process that can’t be fully explained at the transcriptomic level only.

Grain Amaranths Are Defoliation Tolerant Crop Species Capable of Utilizing Stem and Root Carbohydrate Reserves to Sustain Vegetative and Reproductive Growth after Leaf Loss

“…It is shown that grain yield in amaranth was not reduced after the mechanical removal (by hole punching) of 20-to-100% of its leaves at the pre-flowering stage. This study complemented previous reports describing the high tolerance to defoliation shown by grain amaranths [20], [36]. Moreover, the results herewith shown indicate that tolerance may be genetically determined, since different degrees of tolerance between two grain amaranth species examined were observed.…”

“…The trays were maintained in a growth chamber kept at 26°C and 75% relative humidity (R.H.). Amaranth plantlets were subsequently transplanted to 12-L plastic pots, containing a sterile substrate [20], 21-days after germination. They were fertilized once, one week after transplant, with 400 mL of a 20: 10: 20 (N: P: K) nutrient soil drench solution prepared according to the manufacturer's instructions (Peters Professional; Scotts-Sierra Horticultural Products, Marysville, OH, USA).…”

“…reversible inter-conversion between sucrose, hexoses and starch) [16], [17], [18], [19]. Recent investigations have also begun to reveal some biochemical and genetic mechanisms triggered in response to defoliation in diverse plant species [20], [21], [22], [23]. In Sesbania and Populus , physical leaf damage alters the pattern of resource allocation to various vegetative and reproductive organs [24], [25].…”

Alteration of plant primary metabolism in response to insect herbivory

“…1A). Similarly, in grain amaranth (Amaranthus cruentus), foliar herbivory induced a local increase in cytoplasmic invertase and amylolytic enzyme activities (Castrillon-Arbelaez et al, 2012). Furthermore, this study showed lower concentrations of monosaccharides, Suc, and starch in local tissues in the days after herbivore infestation.…”

“…Although both approaches generate large amounts of data, they are also inherently limited. For example, Castrillon-Arbelaez et al (2012) found little correlation between transcript abundance and enzymatic activities when studying herbivore-induced changes in carbohydrate metabolism. Similarly, Coppola et al (2013), from among a thousand differentially expressed transcripts and 87 differentially abundant proteins, found only three transcript-protein matches in herbivoreattacked tomato leaves.…”