A mutation in amino acid permease AAP6 reduces the amino acid content of the Arabidopsis sieve elements but leaves aphid herbivores unaffected

Abstract

The aim of this study was to investigate the role of the amino acid permease gene AAP6 in regulating phloem amino acid composition and then to determine the effects of this altered diet on aphid performance. A genotype of Arabidopsis thaliana (L.) was produced in which the function of the amino acid permease gene AAP6 (At5g49630) was abolished. Plants homozygous for the insertionally inactivated AAP6 gene had a significantly larger mean rosette width than the wild type and a greater number of cauline leaves. Seeds from the aap6 mutant were also significantly larger than those from the wild-type plants. Sieve element (SE) sap was collected by aphid stylectomy and the amino acids derivatized, separated, and quantified using Capillary Electrophoresis with Laser Induced Fluorescence (CE-LIF). In spite of the large variation across samples, the total amino acid concentration of SE sap of the aap6 mutant plants was significantly lower than that of the wild-type plants. The concentrations of lysine, phenylalanine, leucine, and aspartic acid were all significantly lower in concentration in the aap6 mutant plants compared with wild-type plants. This is the first direct demonstration of a physiological role for an amino acid transporter in regulating SE composition in vivo. The amino acid availability in sieve element sap is thought to be the major limiting factor for aphid growth and reproduction. Despite the changes in their diet, the aphid Myzus persicae (Sulzer) displayed only small changes in feeding behaviour on mutant plants when measured using the Electronic Penetration Graph (EPG) technique. Salivation by the aphid into the SE (E1 phase) was increased on mutant plants but there was no significant effect on other feeding EPG behaviours, or in the rate of honeydew production. Consistent with the small effect on aphid feeding behaviour, there was only a small effect of reduced sieve element amino acid concentration on aphid reproduction. The data are discussed in relation to the regulation of phloem composition and the role of phloem amino acids in regulating aphid performance.

The Amino Acid Permeases AAP3 and AAP6 Are Involved in Root-Knot Nematode Parasitism of Arabidopsis

“…The aromatic and neutral amino acid transporter AtANT1 affects the aphid-Arabidopsis relationship by influencing the ingestion rate of the aphid (Hunt et al 2006). AAP6 also has slight effects on aphid parasitism as measured by increased salivation and reduced reproduction (Hunt et al 2010). The more severe effects we observe for RKN are most likely due to the type of tissue infected (roots for RKN versus aerial tissue for aphids) and the fact that RKN establish giant cells to feed from rather than directly tapping into the phloem like aphids.…”

“…Based on these localization patterns, it is believed that these transporters are involved in the long-distance transport of amino acids. Additionally, it was demonstrated that the sieve element sap of an aap6 mutant had reduced overall amino acid content, with significantly less aspartic acid, leucine, lysine, and phenylalanine (Hunt et al 2010).…”

The Phosphorylated Pathway of Serine Biosynthesis Is Essential Both for Male Gametophyte and Embryo Development and for Root Growth in Arabidopsis

“…Synthesis of amino acids takes place mainly in mature roots and source leaves, which export N through the phloemxylem system to supply sinks, such as flowers and seeds (Lam et al, 1996). Specifically, Ser is easily transported through the phloem (Riens et al, 1991;Hunt et al, 2010). This would imply that the Ser synthesized in photosynthetic cells through the photorespiratory pathway could be supplied to nonphotosynthetic organs.…”

Plant N Fluxes and Modulation by Nitrogen, Heat and Water Stresses: A Review Based on Comparison of Legumes and Non Legume Plants

“…Nitrogenous compounds in phloem are similar to those in xylem but more concentrated (5 to 40-fold, Pate et al, 1975). Their concentration varies among plant species, from around 0.1 mol m -3 (Hunt et al, 2010), to over 1.2 mol m -3 (Faria et al, 2007). Aspartate and glutamate and their corresponding amides, asparagine and glutamine often predominates (Girousse et al, 1996;Hunt et al, 2010;Sanders et al, 2009).…”

“…Their concentration varies among plant species, from around 0.1 mol m -3 (Hunt et al, 2010), to over 1.2 mol m -3 (Faria et al, 2007). Aspartate and glutamate and their corresponding amides, asparagine and glutamine often predominates (Girousse et al, 1996;Hunt et al, 2010;Sanders et al, 2009). The relative concentrations of threonine, histidine, tryptophane, and valine vary between plant species.…”