Up-regulation of abscisic acid signaling pathway facilitates aphid xylem absorption and osmoregulation under drought stress

Abstract

The activation of the abscisic acid (ABA) signaling pathway reduces water loss from plants challenged by drought stress. The effect of drought-induced ABA signaling on the defense and nutrition allocation of plants is largely unknown. We postulated that these changes can affect herbivorous insects. We studied the effects of drought on different feeding stages of pea aphids in the wild-type A17 of Medicago truncatula and ABA signaling pathway mutant sta-1. We examined the impact of drought on plant water status, induced plant defense signaling via the abscisic acid (ABA), jasmonic acid (JA), and salicylic acid (SA) pathways, and on the host nutritional quality in terms of leaf free amino acid content. During the penetration phase of aphid feeding, drought decreased epidermis/mesophyll resistance but increased mesophyll/phloem resistance of A17 but not sta-1 plants. Quantification of transcripts associated with ABA, JA and SA signaling indicated that the drought-induced up-regulation of ABA signaling decreased the SA-dependent defense but increased the JA-dependent defense in A17 plants. During the phloem-feeding phase, drought had little effect on the amino acid concentrations and the associated aphid phloem-feeding parameters in both plant genotypes. In the xylem absorption stage, drought decreased xylem absorption time of aphids in both genotypes because of decreased water potential. Nevertheless, the activation of the ABA signaling pathway increased water-use efficiency of A17 plants by decreasing the stomatal aperture and transpiration rate. In contrast, the water potential of sta-1 plants (unable to close stomata) was too low to support xylem absorption activity of aphids; the aphids on sta-1 plants had the highest hemolymph osmolarity and lowest abundance under drought conditions. Taken together this study illustrates the significance of cross-talk between biotic-abiotic signaling pathways in plant-aphid interaction, and reveals the mechanisms leading to alter aphid fecundity in water stresses plants.

Keywords: Abscisic acid; Acyrthosiphon pisum; Medicago truncatula; drought; feeding behavior; jasmonic acid; osmoregulation; resistance; salicylic acid; xylem absorption..

Fig. 1.

Numbers of pea aphids per plant when fed on wild-type A17 and sta-1 (sensitivity-to-ABA) mutant plants grown under well-watered (water) and drought-stressed (drought) conditions. Each value is the mean (±SE) of 12 replicates. Significant differences at P<0.05 are indicated by asterisks. (This figure is available at JXB online.)

Fig. 2.

Electrical penetration graph (EPG) results for pea aphids feeding for 12h on A17 and the sta-1 mutant plants grown under well-watered (water) or drought conditions. (A) Minimum C before E1; (B) number of probes <3min before first E1; (C) time to first E1; (D) time to first E2; (E) time to first G phase; (F) time spent in the xylem phase; and (G) time spent in the phloem phase. Each value is the mean (±SE) of 24 biological replicates. Different lower case letters indicate significant differences between water treatments within the same genotype. Different upper case letters indicate significant differences between genotypes within the same water treatment as determined by Tukey’s multiple range test at P<0.05.

Fig. 3.

ABA content and relative expression of the downstream ABA-responsive protein gene (ABR) for two M. truncatula genotypes grown under well-watered (water) or drought conditions with and without pea aphid infestation. Each value represents the mean (±SE) of four replicates. Different lower case letters indicate significant differences among the combinations of aphid treatment and water treatment within the same genotype. Different upper case letters indicate significant differences between genotypes within the same water treatment and aphid treatment as determined by Tukey’s multiple range test at P<0.05.

Fig. 4.

SA content and expression of genes involved in the SA signaling pathway in two Medicago truncatula genotypes grown under well-watered or drought conditions with and without pea aphid infestation. (a) SA content; (b) pathogenesis-related protein (PR); (c) β-1,3-glucanase (BGL); and (d) endochitinase (CHTN) expression. Each value is the mean (±SE) of eight replicates. Different lower case letters indicate significant differences among the combinations of aphid treatment and water treatment within the same genotype. Different upper case letters indicate significant differences between genotypes within the same water treatment and aphid treatment as determined by Tukey’s multiple range test at P<0.05.

Fig. 5.

Key metabolites and relative expression of key genes involved in the JA signaling pathway for two M. truncatula genotypes grown under well-watered or drought conditions with and without pea aphid infestation. (A) (+)-12-oxophytodienoic acid (OPDA) content; (b) JA content; (c) 12-OPDA reductase (OPR) expression; and (d) cysteine proteinase inhibitor (PI) expression. Each value represents the mean (±SE) of eight replicates. Different lower case letters indicate significant differences among the combinations of aphid treatment and water treatment within the same genotype. Different upper case letters indicate significant differences between genotypes within the same water treatment and aphid treatment as determined by Tukey’s multiple range test at P<0.05.

Fig. 6.

N concentration and phloem amino acid concentration for two M. truncatula genotypes grown under well-watered or drought conditions without pea aphid infestation. Significant differences at P<0.05 are indicated by asterisks.

Fig. 7.

Gas exchange parameters and water status in two Medicago truncatula genotypes grown under well-watered and drought conditions with and without pea aphid infestation. (A) Stomatal conductance; (B) transpiration rate; (C) water-use efficiency (D) water potential; and (E) relative water content. Each value represents the mean (±SE) of eight replicates. Different lower case letters indicate significant differences among the combinations of aphid treatment and water treatment within the same genotype. Different upper case letters indicate significant differences between genotypes within the same water treatment and aphid treatment as determined by Tukey’s multiple range test at P<0.05.

Fig. 8.

Hemolymph osmolarity and relative water content of pea aphids when fed on wild-type A17 and the sta-1 (sensitivity-to-ABA) mutant plants grown under well-watered (water) and drought stress conditions. (A) Hemolymph osmolarity; (B) relative water content. Different lower case letters indicate significant differences between water treatments within the same genotype. Different upper case letters indicate significant differences between genotypes within the same water treatment as determined by Tukey’s multiple range test at P<0.05.

Fig. 9.

A model summarizing the effects of the up-regulated ABA signaling pathway on aphid feeding in the M. truncatula–pea aphid system under drought stress. ≡indicates that drought-induced up-regulation of the ABA signaling pathway did not affect the N nutrition of plants.