Assessment of Local and Systemic Changes in Plant Gene Expression and Aphid Responses during Potato Interactions with Arbuscular Mycorrhizal Fungi and Potato Aphids
Abstract
:1. Introduction
2. Results
2.1. Impact of Two Levels of AM Fungal Root Colonization on Potato Aphid Fitness
2.2. Plant Gene Expression after 24 h of Potato Aphid Herbivory at Two Levels of AM Fungal Root Colonization
2.3. Plant Gene Expression after 10 Days of Potato Aphid Herbivory at Two Levels of AM Fungal Root Colonization
3. Discussion
4. Materials and Methods
4.1. Plant Growth Conditions
4.2. Root Inoculation with the AM Fungus Rhizophagus Intraradices
4.3. Shoot Infestation with Potato Aphids
4.4. Investigating the Impact of AM Fungus Root Colonization on Potato Aphid Fitness
4.5. RNA Isolation and cDNA Synthesis
4.6. Determining Changes in Plant Gene Expression during Aphid–Plant–AM Fungus Interactions
4.7. Statistical Analyses
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Smith, S.E.; Read, D.J. Mycorrhizal Symbiosis, 3rd ed.; Academic Press: New York, NY, USA; Elsevier Ltd.: London, UK, 2008; p. 800. [Google Scholar]
- Delavaux, C.S.; Smith-Ramesh, L.M.; Kuebbing, S.E. Beyond nutrients: A meta-analysis of the diverse effects of arbuscular mycorrhizal fungi on plants and soils. Ecology 2017, 98, 2111–2119. [Google Scholar] [CrossRef] [PubMed]
- Allen, M.F.; Boosalis, M.G. Effects of 2 species of va-mycorrhizal fungi on drought tolerance of winter-wheat. New Phytol. 1983, 93, 67–76. [Google Scholar] [CrossRef]
- Bothe, H. Arbuscular mycorrhiza and salt tolerance of plants. Symbiosis 2012, 58, 7–16. [Google Scholar] [CrossRef]
- French, K.E. Engineering mycorrhizal symbioses to alter plant metabolism and improve crop health. Front. Microbiol. 2017, 8, 1403. [Google Scholar] [CrossRef]
- Hao, Z.P.; Xie, W.; Chen, B. Arbuscular mycorrhizal symbiosis affects plant immunity to viral infection and accumulation. Viruses 2019, 11, 534. [Google Scholar] [CrossRef] [Green Version]
- Barber, N.A. Arbuscular mycorrhizal fungi are necessary for the induced response to herbivores by Cucumis sativus. J. Plant Ecol. 2013, 6, 171–176. [Google Scholar] [CrossRef]
- Berendsen, R.L.; Pieterse, C.M.J.; Bakker, P. The rhizosphere microbiome and plant health. Trends Plant Sci. 2012, 17, 478–486. [Google Scholar] [CrossRef]
- Campos-Soriano, L.; Garcia-Martinez, J.; Segundo, B.S. The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defence-related genes in rice leaves and confers resistance to pathogen infection. Mol. Plant Pathol. 2012, 13, 579–592. [Google Scholar] [CrossRef]
- Cordier, C.; Pozo, M.J.; Barea, J.M.; Gianinazzi, S.; Gianinazzi-Pearson, V. Cell defense responses associated with localized and systemic resistance to Phytophthora parasitica induced in tomato by an arbuscular mycorrhizal fungus. Mol. Plant-Microbe Interact. 1998, 11, 1017–1028. [Google Scholar] [CrossRef] [Green Version]
- Sanchez-Bel, P.; Troncho, P.; Gamir, J.; Pozo, M.J.; Camanes, G.; Cerezo, M.; Flors, V. The nitrogen availability interferes with mycorrhiza-induced resistance against Botrytis cinerea in tomato. Front. Microbiol. 2016, 7, 1598. [Google Scholar] [CrossRef] [Green Version]
- Rasmann, S.; Bennett, A.; Biere, A.; Karley, A.; Guerrieri, E. Root symbionts: Powerful drivers of plant above- and belowground indirect defenses. Insect Sci. 2017, 24, 947–960. [Google Scholar] [CrossRef] [PubMed]
- Hartley, S.E.; Gange, A.C. Impacts of plant symbiotic fungi on insect herbivores: Mutualism in a multitrophic context. Annu. Rev. Entomol. 2009, 54, 323–342. [Google Scholar] [CrossRef] [PubMed]
- Gehring, C.; Bennett, A. Mycorrhizal fungal-plant-insect interactions: The importance of a community approach. Environ. Entomol. 2009, 38, 93–102. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bennett, A.E.; Alers-Garcia, J.; Bever, J.D. Three-way interactions among mutualistic mycorrhizal fungi, plants, and plant enemies: Hypotheses and synthesis. Am. Nat. 2006, 167, 141–152. [Google Scholar] [CrossRef]
- Koricheva, J.; Gange, A.C.; Jones, T. Effects of mycorrhizal fungi on insect herbivores: A meta-analysis. Ecology 2009, 90, 2088–2097. [Google Scholar] [CrossRef]
- Jung, S.C.; Martinez-Medina, A.; Lopez-Raez, J.A.; Pozo, M.J. Mycorrhiza-induced resistance and priming of plant defenses. J. Chem. Ecol. 2012, 38, 651–664. [Google Scholar] [CrossRef]
- Gange, A.C.; Brown, V.K.; Aplin, D.M. Multitrophic links between arbuscular mycorrhizal fungi and insect parasitoids. Ecol. Lett. 2003, 6, 1051–1055. [Google Scholar] [CrossRef]
- Tao, L.L.; Hunter, M.D.; de Roode, J.C. Microbial root mutualists affect the predators and pathogens of herbivores above ground: Mechanisms, magnitudes, and missing links. Front. Ecol. Evol. 2017, 5, 160. [Google Scholar] [CrossRef] [Green Version]
- Pozo, M.J.; Azcon-Aguilar, C. Unraveling mycorrhiza-induced resistance. Curr. Opin. Plant Biol. 2007, 10, 393–398. [Google Scholar] [CrossRef]
- Song, Y.Y.; Ye, M.; Li, C.Y.; Wang, R.L.; Wei, X.C.; Luo, S.M.; Zeng, R.S. Priming of anti-herbivore defense in tomato by arbuscular mycorrhizal fungus and involvement of the jasmonate pathway. J. Chem. Ecol. 2013, 39, 1036–1044. [Google Scholar] [CrossRef]
- Cameron, D.D.; Neal, A.L.; van Wees, S.C.M.; Ton, J. Mycorrhiza-induced resistance: More than the sum of its parts? Trends Plant Sci. 2013, 18, 539–545. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rasmussen, P.U.; Amin, T.; Bennett, A.E.; Karlsson Green, K.; Timonen, S.; Van Nouhuys, S.; Tack, A.J.M. Plant and insect genetic variation mediate the impact of arbuscular mycorrhizal fungi on a natural plant-herbivore interaction. Ecol. Entomol. 2017, 42, 793–802. [Google Scholar] [CrossRef] [Green Version]
- Gange, A.C.; Stagg, P.G.; Ward, L.K. Arbuscular mycorrhizal fungi affect phytophagous insect specialism. Ecol. Lett. 2002, 5, 11–15. [Google Scholar] [CrossRef] [Green Version]
- Gange, A.C. Species-specific responses of a root- and shoot-feeding insect to arbuscular mycorrhizal colonization of its host plant. New Phytol. 2001, 150, 611–618. [Google Scholar] [CrossRef]
- Gange, A.C.; Bower, E.; Brown, V.K. Positive effects of an arbuscular mycorrhizal fungus on aphid life history traits. Oecologia 1999, 120, 123–131. [Google Scholar] [CrossRef] [PubMed]
- Babikova, Z.; Gilbert, L.; Bruce, T.; Dewhirst, S.Y.; Pickett, J.A.; Johnson, D. Arbuscular mycorrhizal fungi and aphids interact by changing host plant quality and volatile emission. Funct. Ecol. 2014, 28, 375–385. [Google Scholar] [CrossRef] [Green Version]
- Simon, A.L.; Wellham, P.A.D.; Aradottir, G.I.; Gange, A.C. Unravelling mycorrhiza-induced wheat susceptibility to the English grain aphid Sitobion avenae. Sci. Rep. 2017, 7, 46497. [Google Scholar] [CrossRef] [Green Version]
- Maurya, A.K.; Kelly, M.P.; Mahaney, S.M.; Gomez, S.K. Arbuscular mycorrhizal symbiosis alters plant gene expression and aphid weight in a tripartite interaction. J. Plant Interact. 2018, 13, 294–305. [Google Scholar] [CrossRef]
- Meier, A.R.; Hunter, M.D. Mycorrhizae alter toxin sequestration and performance of two specialist herbivores. Front. Ecol. Evol. 2018, 6, 33. [Google Scholar] [CrossRef] [Green Version]
- Adkar-Purushothama, C.R.; Brosseau, C.; Giguere, T.; Sano, T.; Moffett, P.; Perreault, J.P. Small RNA derived from the virulence modulating region of the potato spindle tuber viroid silences callose synthase genes of tomato plants. Plant Cell 2015, 27, 2178–2194. [Google Scholar] [CrossRef] [Green Version]
- Karley, A.J.; Emslie-Smith, M.; Bennett, A.E. Potato aphid Macrosiphum euphorbiae performance is determined by aphid genotype and not mycorrhizal fungi or water availability. Insect Sci. 2017, 24, 1015–1024. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wurst, S.; Dugassa-Gobena, D.; Langel, R.; Bonkowski, M.; Scheu, S. Combined effects of earthworms and vesicular-arbuscular mycorrhizas on plant and aphid performance. New Phytol. 2004, 163, 169–176. [Google Scholar] [CrossRef]
- Babikova, Z.; Gilbert, L.; Randall, K.C.; Bruce, T.J.A.; Pickett, J.A.; Johnson, D. Increasing phosphorus supply is not the mechanism by which arbuscular mycorrhiza increase attractiveness of bean (Vicia faba) to aphids. J. Exp. Bot. 2014, 65, 5231–5241. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Colella, T.; Candido, V.; Campanelli, G.; Camele, I.; Battaglia, D. Effect of irrigation regimes and artificial mycorrhization on insect pest infestations and yield in tomato crop. Phytoparasitica 2014, 42, 235–246. [Google Scholar] [CrossRef]
- Guerrieri, E.; Lingua, G.; Digilio, M.C.; Massa, N.; Berta, G. Do interactions between plant roots and the rhizosphere affect parasitoid behaviour? Ecol. Entomol. 2004, 29, 753–756. [Google Scholar] [CrossRef]
- Babikova, Z.; Gilbert, L.; Bruce, T.J.A.; Birkett, M.; Caulfield, J.C.; Woodcock, C.; Pickett, J.A.; Johnson, D. Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecol. Lett. 2013, 16, 835–843. [Google Scholar] [CrossRef]
- Garzo, E.; Rizzo, E.; Fereres, A.; Gomez, S.K. High levels of arbuscular mycorrhizal fungus colonization on Medicago truncatula reduces plant suitability as a host for pea aphids (Acyrthosiphon pisum). Insect Sci. 2018, 27, 99–112. [Google Scholar] [CrossRef] [Green Version]
- Hempel, S.; Stein, C.; Unsicker, S.B.; Renker, C.; Auge, H.; Weisser, W.W.; Buscot, F. Specific bottom-up effects of arbuscular mycorrhizal fungi across a plant-herbivore-parasitoid system. Oecologia 2009, 160, 267–277. [Google Scholar] [CrossRef] [Green Version]
- Krishna, K.; Suresh, H.; Syamsunder, J.; Bagyaraj, D. Changes in the leaves of finger millet due to VA mycorrhizal infection. New Phytol. 1981, 87, 717–722. [Google Scholar] [CrossRef]
- Wilkinson, T.D.J.; Ferrari, J.; Hartley, S.E.; Hodge, A. Aphids can acquire the nitrogen delivered to plants by arbuscular mycorrhizal fungi. Funct. Ecol. 2019, 33, 576–586. [Google Scholar] [CrossRef] [Green Version]
- Gange, A.C.; West, H.M. Interaction between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. New Phytol. 1994, 128, 79–87. [Google Scholar] [CrossRef]
- Tomczak, V.V.; Müller, C. Influence of arbuscular mycorrhizal stage and plant age on the performance of a generalist aphid. J. Insect Physiol. 2017, 98, 258–266. [Google Scholar] [CrossRef] [PubMed]
- Vos, C.M.; Tesfahun, A.N.; Panis, B.; De Waele, D.; Elsen, A. Arbuscular mycorrhizal fungi induce systemic resistance in tomato against the sedentary nematode Meloidogyne incognita and the migratory nematode Pratylenchus penetrans. Appl. Soil Ecol. 2012, 61, 1–6. [Google Scholar] [CrossRef]
- Bernaola, L.; Cosme, M.; Schneider, R.W.; Stout, M. Belowground inoculation with arbuscular mycorrhizal fungi increases local and systemic susceptibility of rice plants to different pest organisms. Front. Plant Sci. 2018, 9, 747. [Google Scholar] [CrossRef] [PubMed]
- Pangesti, N.; Pineda, A.; Pieterse, C.M.J.; Dicke, M.; van Loon, J.J.A. Two-way plant-mediated interactions between root-associated microbes and insects: From ecology to mechanisms. Front. Plant Sci. 2013, 4, 414. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Song, Y.; Chen, D.; Lu, K.; Sun, Z.; Zeng, R. Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Front. Plant Sci. 2015, 6, 786. [Google Scholar] [CrossRef] [Green Version]
- Schoenherr, A.P.; Rizzo, E.; Jackson, N.; Manosalva, P.; Gomez, S.K. Mycorrhiza-induced resistance in potato involves priming of defense responses against cabbage looper (Noctuidae: Lepidoptera). Environ. Entomol. 2019, 48, 370–381. [Google Scholar] [CrossRef]
- Chen, Y.F.; Randlett, M.D.; Findell, J.L.; Schaller, G.E. Localization of the ethylene receptor ETR1 to the endoplasmic reticulum of Arabidopsis. J. Biol. Chem. 2002, 277, 19861–19866. [Google Scholar] [CrossRef] [Green Version]
- Bleecker, A.B.; Kende, H. Ethylene: A gaseous signal molecule in plants. Annu. Rev. Cell Dev. Biol. 2000, 16, 1–8. [Google Scholar] [CrossRef] [Green Version]
- Chang, C.; Stadler, R. Ethylene hormone receptor action in Arabidopsis. Bioessays 2001, 23, 619–627. [Google Scholar] [CrossRef]
- Mantelin, S.; Bhattarai, K.K.; Kaloshian, I. Ethylene contributes to potato aphid susceptibility in a compatible tomato host. New Phytol. 2009, 183, 444–456. [Google Scholar] [CrossRef]
- Anstead, J.; Samuel, P.; Song, N.; Wu, C.J.; Thompson, G.A.; Goggin, F. Activation of ethylene-related genes in response to aphid feeding on resistant and susceptible melon and tomato plants. Entomol. Exp. Appl. 2010, 134, 170–181. [Google Scholar] [CrossRef]
- Guo, H.M.; Li, H.C.; Zhou, S.R.; Xue, H.W.; Miao, X.X. Cis-12-oxo-phytodienoic acid stimulates rice defense response to a piercing-sucking insect. Mol. Plant 2014, 7, 1683–1692. [Google Scholar] [CrossRef] [Green Version]
- Hilou, A.; Zhang, H.Q.; Franken, P.; Hause, B. Do jasmonates play a role in arbuscular mycorrhiza-induced local bioprotection of Medicago truncatula against root rot disease caused by Aphanomyces euteiches? Mycorrhiza 2014, 24, 45–54. [Google Scholar] [CrossRef]
- Kaling, M.; Schmidt, A.; Moritz, F.; Rosenkranz, M.; Witting, M.; Kasper, K.; Janz, D.; Schmitt-Kopplin, P.; Schnitzler, J.-P.; Polle, A. Mycorrhiza-triggered transcriptomic and metabolomic networks impinge on herbivore fitness. Plant Physiol. 2018, 176, 2639–2656. [Google Scholar] [CrossRef] [Green Version]
- Hamza, R.; Pérez-Hedo, M.; Urbaneja, A.; Rambla, J.L.; Granell, A.; Gaddour, K.; Beltrán, J.P.; Cañas, L.A. Expression of two barley proteinase inhibitors in tomato promotes endogenous defensive response and enhances resistance to Tuta absoluta. BMC Plant Biol. 2018, 18, 24. [Google Scholar] [CrossRef] [PubMed]
- Moran, P.J.; Cheng, Y.F.; Cassell, J.L.; Thompson, G.A. Gene expression profiling of Arabidopsis thaliana in compatible plant-aphid interactions. Arch. Insect Biochem. Physiol. 2002, 51, 182–203. [Google Scholar] [CrossRef] [PubMed]
- Florencio-Ortiz, V.; Novak, O.; Casas, J.L. Local and systemic hormonal responses in pepper (Capsicum annuum L.) leaves under green peach aphid (Myzus persicae Sulzer) infestation. J. Plant Physiol. 2018, 231, 356–363. [Google Scholar] [CrossRef] [PubMed]
- Klingler, J.; Creasy, R.; Gao, L.L.; Nair, R.M.; Calix, A.S.; Jacob, H.S.; Edwards, O.R.; Singh, K.B. Aphid resistance in Medicago truncatula involves antixenosis and phloem-specific, inducible antibiosis, and maps to a single locus flanked by NBS-LRR resistance gene analogs. Plant Physiol. 2005, 137, 1445–1455. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- De Vos, M.; Jander, G. Myzus persicae (green peach aphid) salivary components induce defence responses in Arabidopsis thaliana. Plant Cell Environ. 2009, 32, 1548–1560. [Google Scholar] [CrossRef] [PubMed]
- Dugravot, S.; Brunissen, L.; Letocart, E.; Tjallingii, W.F.; Vincent, C.; Giordanengo, P.; Cherqui, A. Local and systemic responses induced by aphids in Solanum tuberosum plants. Entomol. Exp. Appl. 2007, 123, 271–277. [Google Scholar] [CrossRef]
- Martin-Rodriguez, J.A.; Leon-Morcillo, R.; Vierheilig, H.; Ocampo, J.A.; Ludwig-Muller, J.; Garcia-Garrido, J.M. Ethylene-dependent/ethylene-independent ABA regulation of tomato plants colonized by arbuscular mycorrhiza fungi. New Phytol. 2011, 190, 193–205. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.Y.; Maldonado-Mendoza, I.; Lopez-Meyer, M.; Cheung, F.; Town, C.D.; Harrison, M.J. Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J. 2007, 50, 529–544. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.N.; Yuan, J.H.; Yang, W.; Zhu, L.; Su, C.; Wang, X.D.; Wu, H.Y.; Sun, Z.X.; Li, X. Genome wide identification and expression profiling of ethylene receptor genes during soybean nodulation. Front. Plant Sci. 2017, 8, 859. [Google Scholar] [CrossRef] [Green Version]
- Chen, X.Y.; Kim, J.Y. Callose synthesis in higher plants. Plant Signal Behav. 2009, 4, 489–492. [Google Scholar] [CrossRef] [Green Version]
- Will, T.; van Bel, A.J.E. Physical and chemical interactions between aphids and plants. J. Exp. Bot. 2006, 57, 729–737. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Walling, L.L. Avoiding effective defenses: Strategies employed by phloem-feeding insects. Plant Physiol. 2008, 146, 859–866. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Saheed, S.A.; Cierlik, I.; Larsson, K.A.E.; Delp, G.; Bradley, G.; Jonsson, L.M.V.; Botha, C.E.J. Stronger induction of callose deposition in barley by Russian wheat aphid than bird cherry-oat aphid is not associated with differences in callose synthase or beta-1,3-glucanase transcript abundance. Physiol. Plant. 2009, 135, 150–161. [Google Scholar] [CrossRef]
- Kazan, K.; Manners, J.M. MYC2: The master in action. Mol. Plant 2013, 6, 686–703. [Google Scholar] [CrossRef] [Green Version]
- Pozo, M.J.; Van Der Ent, S.; Van Loon, L.C.; Pieterse, C.M.J. Transcription factor MYC2 is involved in priming for enhanced defense during rhizobacteria-induced systemic resistance in Arabidopsis thaliana. New Phytol. 2008, 180, 511–523. [Google Scholar] [CrossRef]
- Floss, D.S.; Levy, J.G.; Levesque-Tremblay, V.; Pumplin, N.; Harrison, M.J. DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. USA 2013, 110, E5025–E5034. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kafle, D.; Hanel, A.; Lortzing, T.; Steppuhn, A.; Wurst, S. Sequential above-and belowground herbivory modifies plant responses depending on herbivore identity. BMC Ecol. 2017, 17, 10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Volpe, V.; Chitarra, W.; Cascone, P.; Volpe, M.G.; Bartolini, P.; Moneti, G.; Pieraccini, G.; Di Serio, C.; Maserti, B.; Guerrieri, E.; et al. The association with two different arbuscular mycorrhizal fungi differently affects water stress tolerance in tomato. Front. Plant Sci. 2018, 9, 1480. [Google Scholar] [CrossRef] [PubMed]
- Mai, V.C.; Drzewiecka, K.; Jelen, H.; Narozna, D.; Rucinska-Sobkowiak, R.; Kesy, J.; Floryszak-Wieczorek, J.; Gabrys, B.; Morkunas, I. Differential induction of Pisum sativum defense signaling molecules in response to pea aphid infestation. Plant Sci. 2014, 221–222, 1–12. [Google Scholar] [CrossRef]
- Stewart, S.A.; Hodge, S.; Bennett, M.; Mansfield, J.W.; Powell, G. Aphid induction of phytohormones in Medicago truncatula is dependent upon time post-infestation, aphid density and the genotypes of both plant and insect. Arthropod-Plant Interact. 2016, 10, 41–53. [Google Scholar] [CrossRef]
- Murashigue, T.; Skoog, F. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 1962, 15, 473–497. [Google Scholar] [CrossRef]
- Javot, H.; Penmetsa, R.V.; Breuillin, F.; Bhattarai, K.; Noar, R.; Gomez, S.K.; Zhang, Q.; Cook, D.R.; Harrison, M.J. Medicago truncatula mtpt4 mutants reveal role for nitrogen in the regulation of the arbuscule degeneration in arbuscular mycorrhizal symbiosis. Plant J. 2011, 68, 954–965. [Google Scholar] [CrossRef]
- Vierheilig, H.; Coughlan, S.; Wyss, U.R.S.; Piche, Y. Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl. Environ. Microbiol. 1998, 64, 5004–5007. [Google Scholar] [CrossRef] [Green Version]
- McGonigle, T.P.; Miller, M.H.; Evans, D.G.; Fairchild, G.L.; Swan, J.A. A new method which gives an objective measure of colonization of roots by vesicular arbuscular mycorrhizal fungi. New Phytol. 1990, 115, 495–501. [Google Scholar] [CrossRef]
- Dou, H.O.; Xv, K.P.; Meng, Q.W.; Li, G.; Yang, X.H. Potato plants ectopically expressing Arabidopsis thaliana CBF3 exhibit enhanced tolerance to high-temperature stress. Plant Cell Environ. 2015, 38, 61–72. [Google Scholar] [CrossRef]
- Lopez-Raez, J.A.; Verhage, A.; Fernandez, I.; Garcia, J.M.; Azcon-Aguilar, C.; Flors, V.; Pozo, M.J. Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J. Exp. Bot. 2010, 61, 2589–2601. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nie, X.Z.; Singh, R.P.; Tai, G.C.C. Molecular characterization and expression analysis of 1-aminocyclopropane-1-carboxylate oxidase homologs from potato under abiotic and biotic stresses. Genome 2002, 45, 905–913. [Google Scholar] [CrossRef] [PubMed]
- Wiesel, L.; Davis, J.L.; Milne, L.; Fernandez, V.R.; Herold, M.B.; Williams, J.M.; Morris, J.; Hedley, P.E.; Harrower, B.; Newton, A.C.; et al. A transcriptional reference map of defence hormone responses in potato. Sci. Rep. 2015, 5, 15229. [Google Scholar] [CrossRef] [Green Version]
- Gao, L.L.; Anderson, J.P.; Klingler, J.P.; Nair, R.M.; Edwards, O.R.; Singh, K.B. Involvement of the octadecanoid pathway in bluegreen aphid resistance in Medicago truncatula. Mol. Plant-Microbe Interact. 2007, 20, 82–93. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 2001, 25, 402–408. [Google Scholar] [CrossRef] [PubMed]
- Nicot, N.; Hausman, J.F.; Hoffmann, L.; Evers, D. Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. J. Exp. Bot. 2005, 56, 2907–2914. [Google Scholar] [CrossRef]
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Rizzo, E.; Sherman, T.; Manosalva, P.; Gomez, S.K. Assessment of Local and Systemic Changes in Plant Gene Expression and Aphid Responses during Potato Interactions with Arbuscular Mycorrhizal Fungi and Potato Aphids. Plants 2020, 9, 82. https://doi.org/10.3390/plants9010082
Rizzo E, Sherman T, Manosalva P, Gomez SK. Assessment of Local and Systemic Changes in Plant Gene Expression and Aphid Responses during Potato Interactions with Arbuscular Mycorrhizal Fungi and Potato Aphids. Plants. 2020; 9(1):82. https://doi.org/10.3390/plants9010082
Chicago/Turabian StyleRizzo, Eric, Tyler Sherman, Patricia Manosalva, and S. Karen Gomez. 2020. "Assessment of Local and Systemic Changes in Plant Gene Expression and Aphid Responses during Potato Interactions with Arbuscular Mycorrhizal Fungi and Potato Aphids" Plants 9, no. 1: 82. https://doi.org/10.3390/plants9010082