Abstract
The phloem-feeding by greenbug (Schizaphis graminum) elicits unique interactions with their host plants. To investigate the expression profiles of sorghum genes responsive to greenbug feeding, two subtractive cDNA libraries were constructed through different combinatorial subtractions in a strong greenbug resistance sorghum M627 line and a susceptible Tx7000 line with or without greenbug infestation. A total of 3,508 cDNAs were selected from the two cDNA libraries, and subsequent cDNA microarray and northern blot analyses were performed for identification of sorghum genes responsive to greenbugs. In total, 157 sorghum transcripts were identified to be differentially expressed by greenbug feeding. The greenbug responsive genes were isolated and classified into nine categories according to the functional roles in plant metabolic pathways, such as defense, signal transduction, cell wall fortification, oxidative burst/stress, photosynthesis, development, cell maintenance, abiotic stress, and unknown function. Overall, the profiles of sorghum genes, responsive to greenbug phloem-feeding shared common identities with other expression profiles known to be elicited by diverse stresses, including pathogenesis, abiotic stress, and wounding. In addition to well-known defense related regulators such as salicylic acid, jasmonic acid, and abscisic acid, auxin and gibberellic acid were also involved in mediation of the defense responses against greenbug phloem-feeding in sorghum.
Similar content being viewed by others
Abbreviations
- ABA:
-
Abscisic acid
- ET:
-
Ethylene
- GA:
-
Gibberellic acid
- JA:
-
Jasmonic acid
- ROS:
-
Reactive oxygen species
- SA:
-
Salicylic acid
References
Ahmadi A, Baker DA (2001) The effect of water stress on the activities of key regulatory enzymes of the sucrose to starch pathways in wheat. Plant Growth Regul 35:81–91
Aroca R, Irigoyen JJ, Sanchez-Diaz M (2003) Drought enhances maize chilling tolerance. II Photosynthetic traits and protective mechanisms against oxidative stress. Physiol Plant 117:540–549
Birkett MA, Campbell CAM, Chamberlain K, Guerrieri E, Hick AJ, Martin JL, Matthes M, Napier JA, Petterson J, Pickett JA, Poppy GM, Pow EM, Pye BJ, Smart LE, Wadhams LJ, Woodcock CM (2000) New roles for cis-jasmone as an insect semiochemical and in plant defense. Proc Natl Acad Sci USA 97:9329–9334
Botella MA, Xu Y, Prabha TN, Zhao Y, Narashimhan ML, Wilson KA, Nielsen SS, Bressan RA, Hasegawa PM (1996) Differential expression of soybean cysteine proteinase inhibitor genes during development and in response to wounding and methyl jasmonate. Plant Physiol 112:1201–1210
Dayakar BV, Lin HJ, Chen CH, Ger MJ, Lee BH, Pai CH, Chow D, Huang HE, Hwang SY, Chung MC, Feng TY (2003) Ferredoxin from sweet pepper (Capsicum annuum L.) intensifying harpinpss-mediated hypersensitive responses shows an enhanced production of active oxygen species (AOS). Plant Mol Biol 51:913–924
Deuschle K, Funck D, Forlani G, Stransky H, Biehl A, Leister D, van der Graaff E, Kunze R, Frommer WB (2004) The role of Δ1-pyrroline-5-carboxylate dehydrogenase in proline degradation. Plant Cell 16:3413–3425
Dmitriev AP (2003) Signal molecules for plant defense responses to biotic stress. Russ J Plant Physiol 50:417–425
Doares SH, Navaez-Vasquez J, Conconi A, Ryan CA (1995) Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol 108:1741–1746
Durner J, Shah J, Klessig DF (1997) Salicylic acid and disease resistance in plants. Trends Plant Sci 2:266–274
Ecker JR (1995) The ethylene signal transduction pathway in plants. Science 268:667–675
Felton GW, Korth KL, Bi JL, Wesley SV, Huhman DV, Mathews MC, Murphy JB, Lamb C, Dixon RA (1999) Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory. Curr Biol 9:317–320
Girousse C, Moulia B, Silk W, Bonnemain JL (2005) Aphid infestation causes different changes in carbon and nitrogen allocation in alfalfa stems as well as different inhibitions of longitudinal and radial expansion. Plant Physiol 137:1474–1484
Halitschke R, Schittko U, Porhnert G, Boland W, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata III Fatty acid–amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol 125:711–717
Hammond-Kosack KE, Jones JDG (1996) Resistance gene-dependent plant defense responses. Plant Cell 8:1773–1791
Holland N, Holland D, Helentjaris T, Dhugga KS, Xoconostle-Cazares B, Delmer DP (2000) A comparative analysis of the plant cellulose synthase (CesA) gene family. Plant Physiol 123:1313–1323
Kachroo A, Lapchyk L, Fukushige H, Hildebrand D, Klessig D, Kachroo P (2003) Plastidial fatty acid signaling modulates salicylic acid- and jasmonic acid-mediated defense pathways in the Arabidopsis ssi2 mutant. Plant Cell 15:2952–2965
Kachroo A, Venugopal SC, Lapchyk L, Falcone D, Hildebrand D, Kachroo P (2004) Oleic acid levels regulated by glycerolipid metabolism modulate defense gene expression in Arabidopsis. Proc Natl Acad Sci USA 101:5152–5157
Katsar CS, Paterson AH, Teetes GL, Peterson GC (2002) Molecular analysis sorghum resistance to the greenbug (Homoptera: Aphididae). J Econ Entomol 95:448–457
Kaur S, Gupta AK, Kaur N (1998) Gibberellin A3 reverses the effect of salt stress in chick pea (Cicer arietinun L.) seedlings by enhancing amylase activity and mobilization of starch in cotyledons. Plant Growth Regul 26:85–90
Kawano T (2003) Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Rep 21:829–837
Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: The emerging molecular analysis. Annu Rev Plant Biol 53:299–328
Kobayashi I, Hakuno H (2003) Actin-related defense mechanism to reject penetration attempt by a non-pathogen is maintained in tobacco BY-2 cells. Planta 217:340–345
Li H, Shen JJ, Zheng ZL, Lin Y, Yang Z (2001) The ROP GTPase switch controls multiple developmental processes in Arabidopsis. Plant Physiol 126:670–684
Li L, Steffens JC (2002) Overexpression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance. Planta 215:239–247
Lu H, Rate DN, Song JT, Greenberg JT (2003) ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response. Plant Cell 15:2408–2420
Majoul T, Bancel E, Tribol E, Hamida JB, Branlard G (2004) Proteomic analysis of the effect of heat stress on hexaploid wheat grain: characterization of heat-responsive proteins from non-prolamins fraction. Proteomics 4:505–513
Maleck K, Dietrich RA (1999) Defense on multiple fronts: how do plants cope with diverse enemies? Trends Plant Sci 4:215–219
Mano J, Torii Y, Hayashi SI, Takimoto K, Matsui K, Nakamura K, Inze D, Babiychuk E, Kushnir S, Asada K (2002) The NADPH: quinine oxidoreductase P1-ζ-crystallin in Arabidopsis catalyzes the α, β-hydrogenation of 2-alkenals: detoxification of the lipid peroxide-derived reactive aldehydes. Plant Cell Physiol 43:1445–1455
Mayda E, Marques C, Conejero V, Vera P (2000) Expression of a pathogen-induced gene can be mimicked by auxin insensitivity. Mol Plant Microbe Interact 13:23–31
Miles PW (1999) Aphid saliva. Biol Rev 74:41–85
Minorsky PV (2002) The wall becomes surmountable. Plant Physiol 128:345–353
Moran PJ, Thompson GA (2001) Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol 125:1074–1085
Moran PJ, Cheng Y, Cassell JL, Thompson GA (2002) Gene expression profiling of Arabidopsis thaliana in compatible plant-aphid interactions. Arch Insect Biochem 51:182–203
Morreel K, Ralph J, Lu F, Goeminne G, Busson R, Herdewijn P, Goeman JL, Van der Eycken J, Boerjan W, Messens E (2004) Phenolic profiling of caffeic acid O-methyltransferase-deficient poplar reveals novel benzodioxane oligolignols. Plant Physiol 136:4023–4036
Narusaka Y, Narusaka M, Seki M, Umezawa T, Ishida J, Nakajima M, Enju A, Shinozaki K (2004) Crosstalk in the responses to abiotic and biotic stresses in Arabidopsis: analysis of gene expression in cytochrome P450 gene superfamily by cDNA microarray. Plant Mol Biol 55:327–342
Oh BJ, Ko MK, Kostenyuk I, Shin BC, Kim KS (1999) Coexpression of a defensin gene and a thionin-like gene via different signal transduction pathways in pepper and Colletotrichum gloeosporioides interaction. Plant Mol Biol 41:313–319
Orozco-Cardenas ML, Narvaez-Vasquez, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in Tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13:179–191
Pare PW, Tumlinson JH (1999) Plant volatiles as a defense against insect herbivores. Plant Physiol 121:325–331
Park JA, Cho SK, Kim JE, Chung HS, Hong JP, Hwang B, Hong CB, Kim WT (2003) Isolation of cDNAs differentially expressed in response to drought stress and characterization of the Ca-LEAL1 gene encoding a new family of atypical LEA-like protein homologue in hot pepper (Capsicum annum L.cv. pukang). Plant Sci 165:471–481
Pechan T, Ye L, Chang YM, Mitra A, Lin L, Davis FM, Williams WP, Luthe DS (2000) A unique 33-kD cysteine proteinase accumulates in response to larvar feeding in maize genotypes resistant to fall armyworm and other Lepidoptera. Plant Cell 12:1031–1040
Pena-Cortes H, Albrecht T, Prat S, Weiler EW, Willmitzer L (1993) Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis. Planta 191:123–128
Penninckx IAMA, Thomma BPHJ, Buchala A, Metraux JP, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10:2103–2113
Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5:237–243
Powell G (2005) Intracellular salivation is the aphid activity associated with inoculation of non-persistently transmitted viruses. J Gen Virol 86:469–472
Reymond P, Farmer EE (1998) Jasmonate and salicylate as global signals for defense gene expression. Curr Opin Plant Biol 1:404–411
Riccardi F, Gazeau P, de Vienne D, Zivy M (1998) Protein changes in response to progressive water deficit in maize. Plant Physiol 117:1253–1263
Ryan CA (2000) The systemin signaling pathway: differential activation of plant defensive genes. Biochim Biophys Acta 1477:112–121
Ryan CA, Pearce G (2003) Systemin: a functionally defined family of peptide signals that regulate defensive genes in Solanaceae species. Proc Natl Acad Sci USA 100:14577–14580
Salzman RA, Brady JA, Finlayson SA, Buchanan CD, Summer EJ, Sun F, Klein PE, Klein RR, Pratt LH, Cordonnier-Pratt MM, Mullet JE (2005) Transcriptional profiling of sorghum induced by methyl jasmonate, salicylic acid, and aminocyclopropane carboxylic acid reveals cooperative regulation and novel gene responses. Plant Physiol 138:352–368
Seo HS, Song JT, Cheong JJ, Lee YH, Lee YW, Hwang IG, Lee JS, Choi YD (2001) Jasmonic acod carboxyl methyltransferase: a key enzyme for jasmonate-regulated plant responses. Proc Natl Acad Sci USA 98:4788–4793
Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97:11655–11660
Schilmiller AL, Howe GA (2005) Systemic signaling in the wound response. Curr Opin Plant Biol 8:369–377
Shields JM, Pruitt K, McFall A, Shaub A, Der CJ (2000) Understanding Ras: ‘it ain’t over ‘til it’s over’. Trends Cell Biol 10:147–154
Shufran KA, Burd JD, Anstead JA, Lushal G (2000) Mitochondrial DNA sequence divergence among greenbug (Homoptera: Aphididae) biotypes: evidence for host-adapted races. Insect Mol Biol 9:179–184
Silvente S, Camas A, Lara M (2003) Molecular cloning of the cDNA encoding aspartate aminotransferase from bean root nodules and determination of its role in nodule nitrogen metabolism. J Exp Bot 54:1545–1551
Stone BS, Shufran RA, Wilde GE (2000) Life history of multiple clones of insecticide resistant and susceptible greenbug Schizaphis graminum (Homoptera: Aphididae). J Econ Entomol 93:971–974
Stotz HU, Kroymann J, Mitchell-Olds T (1999) Plant-insect interactions. Curr Opin Plant Biol 2:268–272
Ting Lee ML, Kuo FC, Whitmore GA, Sklar J (2000) Importance of replication in microarray gene expression studies: statistical methods and evidence from repetitive cDNA hybridizations. Proc Natl Acad Sci USA 97:9834–9839
Tuinstra MR, Wilde GE, Kriegshaauser T (2001) Genetic analysis of biotype I greenbug resistance in sorghum. Euphytica 121:87–91
Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14:S153–S164
Vignols F, Jose-Estanyol M, Caparros-Ruiz D, Rigau J, Puig-domenech P (1999) Involvement of a maize proline-rich protein in secondary cell wall formation as deduced from its specific mRNA localization. Plant Mol Biol 39:945–952
Voelckel C, Weiser WW, Baldwin IT (2004) An analysis of plant-aphid interactions by different microarray hybridization strategies. Mol Ecol 13:3187–3195
Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216
Wang KLC, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14:S131–S151
Watanabe T, Kitagawa H (2000) Photosynthesis and translocation of assimilates in rice plants following phloem feeding by the planthopper Nilaparvata lugens (Homoptera: Delphacidae). J Econ Entomol 93:1192–1198
Yoshimura S, Yamanuchi U, Katayose Y, Toki S, Wang ZX, Kono I, Kurata N, Yano M, Iwata N, Sasaki T (1998) Exppression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proc Natl Acad Sci USA 95:1663–1668
Zhu-Salzman K, Salzman S, Ahn JE, Koiwa H (2004) Transcriptional regulation of sorghum defense determinants against a phloem-feeding aphid. Plant Physiol 134:420–431
Zhu-Salzman K, Bi JL, Liu TX (2005) Molecular strategies of plant defense and insect counter-defense. Insect Sci 12:3–15
Acknowledgements
We thank Dr. Chuck Tauer of Oklahoma State University for the provision of isotope research facilities and Ms. Angela Phillips for her assistance in the microarray preparation. We also thank Dr. Ji-Young Kim and Soo-Yeon Park for their assistance and technical support. This research was funded by the US Department of Agriculture, Agricultural Research Service.
Author information
Authors and Affiliations
Corresponding author
Additional information
Mention of a trademark or proprietary product does not constitute a guarantee or warranty of a product by the U.S. Department of Agriculture and does not imply its approval to the exclusion of other products that may also be suitable.
Rights and permissions
About this article
Cite this article
Park, SJ., Huang, Y. & Ayoubi, P. Identification of expression profiles of sorghum genes in response to greenbug phloem-feeding using cDNA subtraction and microarray analysis. Planta 223, 932–947 (2006). https://doi.org/10.1007/s00425-005-0148-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-005-0148-1