Hunt, E. (Emma), Gattolin, Stefano, Newbury, H. J., Bale, J. S. (Jeffrey S.), Tseng, Hua-Ming, Barrett, D. A. (David A.) and Pritchard, J. (Jeremy). (2010) A mutation in amino acid permease AAP6 reduces the amino acid content of the Arabidopsis sieve elements but leaves aphid herbivores unaffected. Journal of Experimental Botany, Vol.61 (No.1). pp. 55-64. ISSN 0022-0957

PDF WRAP_Gattolin_Mutation_amino.pdf - Requires a PDF viewer such as GSview, Xpdf or Adobe Acrobat Reader Download (394Kb)

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.

Item Type:	Journal Article
Subjects:	Q Science > QK Botany S Agriculture > SB Plant culture
Divisions:	Faculty of Science > Life Sciences (2010- ) > Biological Sciences ( -2010)
Library of Congress Subject Headings (LCSH):	Arabidopsis thaliana, Capillary electrophoresis, Green peach aphid, Sieve elements -- Research, Amino acids -- Metabolism
Journal or Publication Title:	Journal of Experimental Botany
Publisher:	Oxford University Press
ISSN:	0022-0957
Date:	January 2010
Volume:	Vol.61
Number:	No.1
Page Range:	pp. 55-64
Identification Number:	10.1093/jxb/erp274
Status:	Peer Reviewed
Access rights to Published version:	Open Access
References:	Bennett MJ, Marchant A, Green HG, Ward SP, Millner PA, Walker AR, Schulz B, Feldmann KA. Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science (1996) 273:948–950.[Abstract] Bi JL, Castle SJ, Toscano NC. Amino acid fluctuations in young and old orange trees and their influence on glassy-winged sharpshooter (Homalodisca vitripennis) population densities. Journal of Chemical Ecology (2007) 33:1692–1706.[CrossRef][Web of Science][Medline] Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Gorlach J. Growth stage-based phenotypic analysis of arabidopsis: a model for high throughput functional genomics in plants. The Plant Cell (2001) 13:1499–1510.[Abstract/Free Full Text] Chen LS, Bush DR. LHT1, lysine- and histidine-specific amino acid transporter in Arabidopsis. Plant Physiology (1997) 115:1127–1134.[Abstract] Chen LS, Ortiz-Lopez A, Jung A, Bush DR. ANT1, an aromatic and neutral amino acid transporter in Arabidopsis. Plant Physiology (2001) 125:1813–1820.[Abstract/Free Full Text] Deeken R, Geiger D, Fromm J, Koroleva O, Ache P, Langenfeld-Heyser R, Sauer N, May ST, Hedrich R. Loss of the AKT2/3 potassium channel affects sugar loading into the phloem of Arabidopsis. Planta (2002) 216:334–344.[CrossRef][Web of Science][Medline] Douglas AE. The nutritional physiology of aphids. Advances in Insect Physiology (2003) 31:73–140.[CrossRef][Web of Science] Douglas AE. Phloem-sap feeding by animals: problems and solutions. Journal of Experimental Botany (2006) 57:747–754.[Abstract/Free Full Text] Douglas AE, Minto LB, Wilkinson TL. Quantifying nutrient production by the microbial symbionts in an aphid. Journal of Experimental Biology (2001) 204:349–358.[Abstract] Doering-Saad C, Newbury HJ, Bale JS, Pritchard J. Use of aphid stylectomy and RT-PCR for the detection of transporter mRNAs in sieve elements. Journal of Experimental Botany (2002) 53:631–637.[Abstract/Free Full Text] Doering-Saad C, Newbury HJ, Couldridge CE, Bale JS, Pritchard J. A phloem-enriched cDNA library from Ricinus: insights into phloem function. Journal of Experimental Botany (2006) 57:3183–3193.[Abstract/Free Full Text] Downing N, Unwin DM. A new method for cutting the mouthparts of feeding aphids, and for collecting plant sap. Physiological Entomology (1977) 2:275–277.[CrossRef][Web of Science] Dündar E, Bush DR. BAT1, a bidirectional amino acid transporter in Arabidopsis. Planta (2009) 229:1047–1056.[CrossRef][Web of Science][Medline] Feinberg AP, Vogelstein B. A technique for radiolabeling dna restriction endonuclease fragments to high specific activity. Analytical Biochemistry (1983) 132:6–13.[CrossRef][Web of Science][Medline] Fischer WN, Kwart M, Hummel S, Frommer WB. Substrate specificity and expression profile of amino acid transporters (AAPs) in Arabidopsis. Journal of Biological Chemistry (1995) 270:16315–16320.[Abstract/Free Full Text] Fischer WN, Andre B, Rentsch D, Krolkiewicz S, Tegeder M, Breitkreuz K, Frommer WB. Amino acid transport in plants. Trends in Plant Science (1998) 3:188–195.[CrossRef][Web of Science] Fischer WN, Loo DDF, Koch W, Ludewig U, Boorer KJ, Tegeder M, Rentsch D, Wright EM, Frommer WB. Low and high affinity amino acid H+-cotransporters for cellular import of neutral and charged amino acids. The Plant Journal (2002) 29:717–731.[CrossRef][Web of Science][Medline] Frommer WB, Hummel S, Riesmeier JW. Expression cloning in yeast of a cDNA encoding a broad specificity amino acid permease from Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA (1993) 90:5944–5948.[Abstract/Free Full Text] Frommer WB, Hummel S, Unseld M, Ninnemann O. Seed and vascular expression of a high-affinity transporter for cationic amino acids in Arabidopsis. Proceedings of the National Academy of Sciences, USA (1995) 92:12036–12040.[Abstract/Free Full Text] Gattolin S, Newbury HJ, Bale JS, Tseng HM, Barrett DA, Pritchard J. A diurnal component to the variation in sieve tube amino acid content in wheat. Plant Physiology (2008) 147:912–921.[Abstract/Free Full Text] Gaupels F, Buhtz A, Knauer T, Deshmukh S, Waller F, van Bel AJE, Kogel KH, Kehr J. Adaptation of aphid stylectomy for analyses of proteins and mRNAs in barley phloem sap. Journal of Experimental Botany (2008) 59:3297–3306.[Abstract/Free Full Text] Gould N, Thorpe MR, Minchin PEH, Pritchard J, White PJ. Solute is imported to elongating root cells of barley as a pressure driven-flow of solution. Functional Plant Biology (2004) 31:391–397.[CrossRef][Web of Science] Hale BK, Bale JS, Pritchard J, Masters GJ. Effects of host plant drought stress on the performance of the bird cherry-oat aphid, Rhopalosiphum padi (L.): a mechanistic analysis. Ecological Entomology (2003) 28:666–677.[CrossRef][Web of Science] Harrewijn P. Reproduction of the aphid Myzus persicae related to the mineral nutrition of potato plants. Entomologia Experimentalis et Applicata (1970) 13:307–319.[CrossRef][Web of Science] Hirner B, Fischer WN, Rentsch D, Kwart M, Frommer WB. Developmental control of H+/amino acid permease gene expression during seed development of Arabidopsis. The Plant Journal (1998) 14:535–544.[CrossRef][Web of Science][Medline] Hsu LC, Chiou TJ, Chen L, Bush DR. Cloning a plant amino acid transporter by functional complementation of a yeast amino acid transport mutant. Proceedings of the National Academy of Sciences, USA (1993) 90:7441–7445.[Abstract/Free Full Text] Hunt EJ, Pritchard J, Bennett MJ, Zhu X, Barrett DA, Allen T, Bale JS, Newbury HJ. The Arabidopsis thaliana/Myzus persicae model system demonstrates that a single gene can influence the interaction between a plant and a sap-feeding insect. Molecular Ecology (2006) 15:4203–4213.[CrossRef][Medline] Karley AJ, Douglas AE, Parker WE. Amino acid composition and nutritional quality of potato leaf phloem sap for aphids. Journal of Experimental Biology (2002) 205:3009–3018.[Abstract/Free Full Text] Koch W, Kwart M, Laubner M, Heineke D, Stransky H, Frommer WB, Tegeder M. Reduced amino acid content in transgenic potato tubers due to antisense inhibition of the leaf H+/amino acid symporter StAAP1. The Plant Journal (2003) 33:211–220.[CrossRef][Web of Science][Medline] Kwart M, Hirner B, Hummel S, Frommer WB. Differential expression of two related amino acid transporters with differing substrate specificity in Arabidopsis thaliana. The Plant Journal (1993) 4:993–1002.[CrossRef][Web of Science][Medline] Okumoto S, Schmidt R, Tegeder M, Fischer WN, Rentsch D, Frommer WB, Koch W. High affinity amino acid transporters specifically expressed in xylem parenchyma and developing seeds of Arabidopsis. Journal of Biological Chemistry (2002) 277:45338–45346.[Abstract/Free Full Text] Ponder KL, Pritchard J, Harrington R, Bale JS. Difficulties in location and acceptance of phloem sap combined with reduced concentration of phloem amino acids explain lowered performance of the aphid Rhopalosiphum padi on nitrogen deficient barley (Hordeum vulgare) seedlings. Entomologia Experimentalis et Applicata (2000) 97:203–210.[CrossRef][Web of Science] Ponder KL, Pritchard J, Harrington R, Bale JS. Feeding behaviour of the aphid Rhopalosiphum padi (Hemiptera: Aphididae) on nitrogen and water-stressed barley (Hordeum vulgare) seedlings. Bulletin of Entomological Research (2001) 91:125–130.[Web of Science][Medline] Prado E, Tjallingii WF. Effects of previous plant infestation on sieve element acceptance by two aphids. Entomologia Experimentalis et Applicata (1997) 82:189–200.[CrossRef][Web of Science] Pritchard J. Aphid stylectomy reveals an osmotic step between sieve tube and cortical cells in barley roots. Journal of Experimental Botany (1996) 47:1519–1524.[Abstract/Free Full Text] Pritchard J. Solute transport in the phloem. In: Plant solute transport—Flowers TJ, Yeo AR, eds. (2007) Oxford, UK: Blackwell Publishing. 235–309. Rentsch D, Boorer KJ, Frommer WB. Structure and function of plasma membrane amino acid, oligopeptide and sucrose transporters from higher plants. Journal of Membrane Biology (1998) 162:177–190.[CrossRef][Web of Science][Medline] Rentsch D, Hirner B, Schmelzer E, Frommer WB. Salt stress-induced proline transporters and salt stress-repressed broad specificity amino acid permeases identified by suppression of a yeast amino acid permease-targeting mutant. The Plant Cell (1996) 8:1437–1446.[Abstract] Sandström J. Nutritional quality of phloem sap in relation to host plant alternation in the bird cherry-oat aphid. Chemoecology (2000) 10:17–24.[CrossRef][Web of Science] Schmidt R, Stransky H, Koch W. The amino acid permease AAP8 is important for early seed development in Arabidopsis thaliana. Planta (2007) 12:805–813. Shakesby AJ, Wallace IS, Isaacs HV, Pritchard J, Roberts DM, Douglas AE. A water-specific aquaporin involved in aphid osmoregulation. Insect Biochemistry and Molecular Biology (2009) 39:1–10.[CrossRef][Web of Science][Medline] Slewinski TL, Meeley R, Braun DM. Sucrose transporter1 functions in phloem loading in maize leaves. Journal of Experimental Botany (2009) 60:881–892.[Abstract/Free Full Text] Stadler R, Sauer N. Arabidopsis thaliana AtSUC2 gene is specifically expressed in companion cells. Botanica Acta (1996) 109:299–306.[Web of Science] Tegeder M, Tan Q, Grennan AK, Patrick JW. Amino acid transporter expression and localization studies in pea (Pisum sativum). Functional Plant Biology (2007) 34:1019–1028.[CrossRef][Web of Science] Tjallingii WF, Hogen Esch T. Fine structure of aphid stylet route in plant tissues in correlation with EPG signals. Physiological Entomology (1993) 18:317–328.[CrossRef][Web of Science] Tomos AD, Hinde P, Richardson P, Pritchard J, Fricke W. Microsampling and measurements of solutes in single cells. In: Plant cell biology: a practical approach—Harris N, Oparka KJ, eds. (1994) Oxford University Press. 297–314. Tosh CR, Powell G, Holmes ND, Hardie J. Reproductive response of generalist and specialist aphid morphs with the same genotype to plant secondary compounds and amino acids. Journal of Insect Physiology (2003) 49:1173–1182.[CrossRef][Web of Science][Medline] Van Emden HF. Studies on the relations of insect and host plant. III. A comparison of the reproduction of Brevicoryne brassicae and Myzus persicae (Homoptera: Aphididae) on Brussel's sprout plants supplied with different rates of nitrogen and potassium. Entomologia Experimentalis et Applicata (1966) 9:444–460.[CrossRef][Web of Science] Van Helden M, Tjallingii WF. Tissue localization of lettuce resistance to the aphid Nasonovia ribisnigri using electrical penetration graphs. Entomologia Experimentalis et Applicata (1993) 68:269–278.[CrossRef][Web of Science] Will T, Tjallingii WF, Thonnessen A, van Bel AJE. Molecular sabotage of plant defense by aphid saliva. Proceedings of the National Academy of Sciences, USA (2007) 104:10536–10541.[Abstract/Free Full Text] Wilkinson TL, Douglas AE. Plant penetration by pea aphids (Acyrthosiphon pisum) of different plant range. Entomologia Experimentalis et Applicata (1998) 87:43–50. Wilkinson TL, Douglas AE. Phloem amino acids and the host plant range of the polyphagous aphid, Aphis fabae. Entomologia Experimentalis et Applicata (2003) 106:103–113. Williams LE, Miller AJ. Transporters responsible for the uptake and partitioning of nitrogenous solutes. Annual Review of Plant Physiology and Plant Molecular Biology (2001) 52:659–688. Wyatt IJ, White PF. Simple estimation of intrinsic rates from aphids and tertanyxhid mites. Journal of Applied Ecology (1977) 14:757–766. Zhu X, Shaw PN, Pritchard J, Newbury J, Hunt EJ, Barrett DA. Amino acid analysis by micellar electrokinetic chromatography with laser-induced fluorescence detection: Application to nanolitre-volume biological samples from Arabidopsis thaliana and Myzus persicae. Electrophoresis (2005) 26:911–919.
URI:	http://wrap.warwick.ac.uk/id/eprint/2551

Data sourced from Thomson Reuters' Web of Knowledge

Request changes to a record

Actions (login required)

View Item