PvLOX2 silencing in common bean roots impairs arbuscular mycorrhiza-induced resistance without affecting symbiosis establishment
Guadalupe A. Mora-Romero A B , Maria A. Gonzalez-Ortiz A , Francisco Quiroz-Figueroa A , Carlos L. Calderon-Vazquez A , Sergio Medina-Godoy A , Ignacio Maldonado-Mendoza A , Analilia Arroyo-Becerra C , Anahí Perez-Torres D , Fulgencio Alatorre-Cobos D , Federico Sanchez E and Melina Lopez-Meyer A F
+ Author Affiliations
- Author Affiliations
A Instituto Politecnico Nacional CIIDIR-Sinaloa, Depto. Biotecnologia Agricola, Blvd. Juan de Dios Batiz Paredes 250, Guasave PO 81101, Mexico.
B Universidad de Occidente, Instituto de Investigacion en Ambiente y Salud, Los Mochis PO 81200, Mexico.
C Instituto Politecnico Nacional CIBA-Tlaxcala, Ex-Hacienda San Juan Molino Carretera Estatal Tecuexcomac-Tepetitla Km 1.5 Tlaxcala PO 90700, Mexico.
D Unidad de Genomica Avanzada (UGA) Centro de Investigacion y de Estudios Avanzados del IPN, Km. 9.6 Libramiento Norte Carretera Irapuato-Leon, Irapuato PO 36821, Mexico.
E Departamento de Biologia Molecular de Plantas, Instituto de Biotecnologia, Universidad Nacional Autonoma de Mexico, Avenuenida Universidad 2001, PO 62210, Mexico.
F Corresponding author. Email: mlopez@ipn.mx
Functional Plant Biology 42(1) 18-30 https://doi.org/10.1071/FP14101
Submitted: 1 April 2014 Accepted: 7 July 2014 Published: 21 August 2014
Abstract
The arbuscular mycorrhizal (AM) symbiosis is an intimate association between specific soil-borne fungi and the roots of most land plants. AM colonisation elicits an enhanced defence resistance against pathogens, known as mycorrhizal-induced resistance (MIR). This mechanism locally and systemically sensitises plant tissues to boost their basal defence response. Although a role for oxylipins in MIR has been proposed, it has not yet been experimentally confirmed. In this study, when the common bean (Phaseolus vulgaris L.) lipoxygenase PvLOX2 was silenced in roots of composite plants, leaves of silenced plants lost their capacity to exhibit MIR against the foliar pathogen Sclerotinia sclerotiorum, even though they were colonised normally. PvLOX6, a LOX gene family member, is involved in JA biosynthesis in the common bean. Downregulation of PvLOX2 and PvLOX6 in leaves of PvLOX2 root-silenced plants coincides with the loss of MIR, suggesting that these genes could be involved in the onset and spreading of the mycorrhiza-induced defence response.
Additional keywords: fungi, RNA silencing, systemic resistance.
References
Ahmad S, Gordon-Weeks R, Picket J, Ton J (2010) Natural variation in priming of basal resistance: from evolutionary origin to agricultural exploitation. Molecular Plant Pathology 11, 817–827.Beckers GJM, Jaskiewicz M, Li Y, Underwood WR, He SY, Zhang S, Conrath U (2009) Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. The Plant Cell 21, 944–953.
| Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsFylurk%3D&md5=f5ca99f04417ffaf3d296c08d15521a0CAS |
Benabdellah K, Merlos M-Á, Azcón-Aguilar C, Ferrol N (2009) GintGRX1, the first characterized glomeromycotan glutaredoxin, is a multifunctional enzyme that responds to oxidative stress. Fungal Genetics and Biology 46, 94–103.
| GintGRX1, the first characterized glomeromycotan glutaredoxin, is a multifunctional enzyme that responds to oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFagtLbK&md5=2c29afbd92cea1d31c7dfc4a1b38df5bCAS | 18955149PubMed |
Campos-Soriano L, García-Martínez J, Segundo BS (2012) The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defence-related genes in rice leaves and confers resistance to pathogen infection. Molecular Plant Pathology 13, 579–592.
| The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defence-related genes in rice leaves and confers resistance to pathogen infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlGhtL3J&md5=e873149e717d9e7e56049e412ecf9f72CAS | 22212404PubMed |
Conrath U (2011) Molecular aspects of defence priming. Trends in Plant Science 16, 524–531.
| Molecular aspects of defence priming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1GgsLfF&md5=e9b635c53dad3af3148acee5a39686baCAS | 21782492PubMed |
Conrath U, Beckers GJM, Flors V, García-Agustín P, Jakab G, Mauch F, Newman M-A, Pieterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B (2006) Priming: getting ready for battle. Molecular Plant-Microbe Interactions 19, 1062–1071.
| Priming: getting ready for battle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht12ht77F&md5=bf25434d2423ab6c30499482bb352fafCAS | 17022170PubMed |
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
| MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisF2ks7w%3D&md5=7834e74ffd464ccc1a77e461f58eded2CAS | 15034147PubMed |
Eiben GH, Slusarenko AJ (1994) Complex spatial and temporal expression of lipoxygenase genes during Phaseolus vulgaris (L.) development. The Plant Journal 5, 123–135.
| Complex spatial and temporal expression of lipoxygenase genes during Phaseolus vulgaris (L.) development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmt1eht78%3D&md5=d91cd6caafb03c86e105f521e17d0b5fCAS |
Estrada-Navarrete G, Alvarado-Affantranger X, Olivares JE, Diaz-Camino C, Santana O, Murillo E, Guillen G, Sanchez-Guevara N, Acosta J, Quinto C, Li D, Gresshoff PM, Sanchez F (2006) Agrobacterium rhizogenes transformation of the Phaseolus spp.: a tool for functional genomics. Molecular Plant-Microbe Interactions 19, 1385–1393.
| Agrobacterium rhizogenes transformation of the Phaseolus spp.: a tool for functional genomics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1yjs73E&md5=a72a2e63828572ae08e1ce7b87191a98CAS | 17153923PubMed |
Feussner I, Wasternack C (2002) The lipoxygenase pathway. Annual Review of Plant Biology 53, 275–297.
| The lipoxygenase pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVWhur4%3D&md5=2cda9f91f20d6ad384cd8fe32436614dCAS | 12221977PubMed |
Fiorilli V, Catoni M, Francia D, Cardinale F, Lanfranco L (2011) The arbuscular mycorrhizal symbiosis reduces disease severity in tomato plants infected by Botrytis cinerea. Journal of Plant Pathology 93, 237–242.
Gallou A, Lucero Mosquera HP, Cranenbrouck S, Suárez JP, Declerck S (2011) Mycorrhiza induced resistance in potato plantlets challenged by Phytophthora infestans. Physiological and Molecular Plant Pathology 76, 20–26.
| Mycorrhiza induced resistance in potato plantlets challenged by Phytophthora infestans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVGqu7rF&md5=4bd85cf670ef2386507f7659d5a2f319CAS |
Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytologist 84, 489–500.
| An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots.Crossref | GoogleScholarGoogle Scholar |
Hao Z, Fayolle L, van Tuinen D, Chatagnier O, Li X, Gianinazzi S, Gianinazzi-Pearson V (2012) Local and systemic mycorrhiza-induced protection against the ectoparasitic nematode Xiphinema index involves priming of defence gene responses in grapevine. Journal of Experimental Botany 63, 3657–3672.
| Local and systemic mycorrhiza-induced protection against the ectoparasitic nematode Xiphinema index involves priming of defence gene responses in grapevine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVShtL%2FK&md5=9cea6dabfa711d1ec83a9d3fb5f55ebfCAS | 22407649PubMed |
Hause B, Maier W, Miersch O, Kramell R, Strack D (2002) Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiology 130, 1213–1220.
| Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVOmsrg%3D&md5=5bb38cc47b96f7308922f92b0c6b1ad1CAS | 12427988PubMed |
Hayashi S, Gresshoff PM, Kinkema M (2008) Molecular analysis of lipoxygenases associated with nodule development in soybean. Molecular Plant-Microbe Interactions 21, 843–853.
| Molecular analysis of lipoxygenases associated with nodule development in soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtlejtbk%3D&md5=9c4f2507f6ed4a3497c08a510f88e43dCAS | 18624647PubMed |
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. California Agricultural Experiment Station Circular 347, 1–32.
Jang IC, Yang SW, Yang JY, Chua NH (2007) Independent and interdependent functions of LAF1 and HFR1 in phytochrome A signaling. Genes & Development 21, 2100–2111.
| Independent and interdependent functions of LAF1 and HFR1 in phytochrome A signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVSgu7jE&md5=557b469f79722765b4ea6742e5e331c0CAS |
Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT (2009) Priming in systemic plant immunity. Science 324, 89–91.
| Priming in systemic plant immunity.Crossref | GoogleScholarGoogle Scholar | 19342588PubMed |
Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA (2008) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proceedings of the National Academy of Sciences of the United States of America 105, 7100–7105.
| COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmt1Gmurc%3D&md5=040ce9f13f6689ea90b84f8fa81af802CAS | 18458331PubMed |
Kohler A, Schwindling S, Conrath U (2002) Benzothiadiazole-induced priming for potentiated responses to pathogen infection, wounding, and infiltration of water into leaves requires the NPR1/NIM1 gene in Arabidopsis. Plant Physiology 128, 1046–1056.
| Benzothiadiazole-induced priming for potentiated responses to pathogen infection, wounding, and infiltration of water into leaves requires the NPR1/NIM1 gene in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit1GqtLo%3D&md5=ca7612119ecae425ed802d58fe932765CAS | 11891259PubMed |
León Morcillo RJ, Ocampo JA, García Garrido JM (2012) Plant 9-lox oxylipin metabolism in response to arbuscular mycorrhiza. Plant Signaling & Behavior 7, 1584–1588.
| Plant 9-lox oxylipin metabolism in response to arbuscular mycorrhiza.Crossref | GoogleScholarGoogle Scholar |
Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. The Plant Journal 50, 529–544.
| Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlsVWms7Y%3D&md5=2084d657d896e4f0f82da9ac4e987b60CAS | 17419842PubMed |
López-Ráez JA, Verhage A, Fernández I, García JM, Azcón-Aguilar C, Flors V, Pozo MJ (2010) Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. Journal of Experimental Botany 61, 2589–2601.
| Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway.Crossref | GoogleScholarGoogle Scholar | 20378666PubMed |
Meier BM, Shaw N, Slusarenko AJ (1993) Spatial and temporal accumulation of defense gene transcripts in bean (Phaseolus vulgaris) leaves in relation to bacteria-induced hypersensitive cell death. Molecular Plant-Microbe Interactions 6, 453–466.
| Spatial and temporal accumulation of defense gene transcripts in bean (Phaseolus vulgaris) leaves in relation to bacteria-induced hypersensitive cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXitFaktL8%3D&md5=ad5a06e2304f61a0c6d70b44201ce3e6CAS | 8400375PubMed |
Mora-Romero GA (2008) Efecto de la micorrización con Glomus intraradices en la tolerancia al moho blanco causado por Sclerotinia sclerotiorum en tres líneas de frijol. MSc Thesis. Instituto Politécnico Nacional, Guasave, Mexico.
Mosblech A, Feussner I, Heilmann I (2009) Oxylipins: structurally diverse metabolites from fatty acid oxidation. Plant Physiology and Biochemistry 47, 511–517.
| Oxylipins: structurally diverse metabolites from fatty acid oxidation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltFWlurc%3D&md5=4ec663f774792d2d5cae5e28d42e0e02CAS | 19167233PubMed |
Noval B, Pérez E, Martínez B, León O, Martínez-Gallardo N, Délano-Frier J (2007) Exogenous systemin has a contrasting effect on disease resistance in mycorrhizal tomato (Solanum lycopersicum) plants infected with necrotrophic or hemibiotrophic pathogens. Mycorrhiza 17, 449–460.
| Exogenous systemin has a contrasting effect on disease resistance in mycorrhizal tomato (Solanum lycopersicum) plants infected with necrotrophic or hemibiotrophic pathogens.Crossref | GoogleScholarGoogle Scholar | 17356854PubMed |
Pastor V, Luna E, Mauch-Mani B, Ton J, Flors V (2013) Primed plants do not forget. Environmental and Experimental Botany 94, 46–56.
| Primed plants do not forget.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1aqsb3O&md5=1152d563f4a755d77b8b7403a92854c8CAS |
Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55, 158–161.
| Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection.Crossref | GoogleScholarGoogle Scholar |
Porta H, Rocha-Sosa M (2000) A Phaseolus vulgaris lipoxygenase gene expressed in nodules and in Rhizobium tropici inoculated roots. Biochimica et Biophysica Acta 1517, 139–142.
| A Phaseolus vulgaris lipoxygenase gene expressed in nodules and in Rhizobium tropici inoculated roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXoslGmsL8%3D&md5=7176dfb7c6ba144e8583ac9a12d91d0bCAS | 11118627PubMed |
Porta H, Rocha-Sosa M (2002) Plant lipoxygenases. Physiological and molecular features. Plant Physiology 130, 15–21.
| Plant lipoxygenases. Physiological and molecular features.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntFOrsL0%3D&md5=86a1c7f3837c64e6fd44611b1456e024CAS | 12226483PubMed |
Porta H, Rueda-Benitez P, Campos F, Colmenero-Flores JM, Colorado JM, Carmona MJ, Covarrubias AA, Rocha-Sosa M (1999) Analysis of lipoxygenase mRNA accumulation in the common bean (Phaseolus vulgaris L.) during development and under stress conditions. Plant & Cell Physiology 40, 850–858.
| Analysis of lipoxygenase mRNA accumulation in the common bean (Phaseolus vulgaris L.) during development and under stress conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlsVOhsbw%3D&md5=13364adb0411fdf95b29430cf43f2b8fCAS |
Porta H, Figueroa-Balderas RE, Rocha-Sosa M (2008) Wounding and pathogen infection induce a chloroplast-targeted lipoxygenase in the common bean (Phaseolus vulgaris L.). Planta 227, 363–373.
| Wounding and pathogen infection induce a chloroplast-targeted lipoxygenase in the common bean (Phaseolus vulgaris L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlOqsLvN&md5=a06f5955b6fa10cefa372e3265d44c73CAS | 17899174PubMed |
Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Current Opinion in Plant Biology 10, 393–398.
| Unraveling mycorrhiza-induced resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXosFGrsbs%3D&md5=ec26e8937a3b944f4cfd310f061049beCAS | 17658291PubMed |
Pozo M, Jung S, López-Ráez J, Azcón-Aguilar C (2010) Impact of arbuscular mycorrhizal symbiosis on plant response to biotic stress: the role of plant defence mechanisms. In ‘Arbuscular mycorrhizas: physiology and function’. (Eds H Koltai, Y Kapulnik) pp. 193–207. (Springer: Dordrecht, The Netherlands)
Riedel T, Groten K, Baldwin IT (2008) Symbiosis between Nicotiana attenuata and Glomus intraradices: ethylene plays a role, jasmonic acid does not. Plant, Cell & Environment 31, 1203–1213.
| Symbiosis between Nicotiana attenuata and Glomus intraradices: ethylene plays a role, jasmonic acid does not.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Sqsb3E&md5=4dcdaf4b621f91bbe4f81293368f1d85CAS |
Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycological Research 105, 1413–1421.
| A new fungal phylum, the Glomeromycota: phylogeny and evolution.Crossref | GoogleScholarGoogle Scholar |
Steadman JR, Powers K, Higgins B (1997) Screening common bean for white mold resistance using detached leaves. Annual Report of the Bean Improvement Cooperative. Bean Improvement Cooperative 40, 140–141.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.
| MEGA6: molecular evolutionary genetics analysis version 6.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVKhurzP&md5=2504364b976e0abdf7079f45f502bdb9CAS | 24132122PubMed |
Valdés-López O, Arenas-Huertero C, Ramírez M, Girard L, Sánchez F, Vance CP, Reyes JL, Hernández G (2008) Essential role of MYB transcription factor: PvPHR1 and microRNA: PvmiR399 in phosphorus-deficiency signalling in common bean roots. Plant, Cell & Environment 31, 1834–1843.
| Essential role of MYB transcription factor: PvPHR1 and microRNA: PvmiR399 in phosphorus-deficiency signalling in common bean roots.Crossref | GoogleScholarGoogle Scholar |
Van der Ent S, Van Wees SCM, Pieterse CMJ (2009) Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 70, 1581–1588.
| Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlGiu7fN&md5=9f7ec9d2dda0297d37304a5772e2b0a9CAS | 19712950PubMed |
Van Wees SCM, Van der Ent S, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Current Opinion in Plant Biology 11, 443–448.
| Plant immune responses triggered by beneficial microbes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpsVamurw%3D&md5=8261c00146d0693f6c3264eaa604a2e7CAS |
Vos C, Schouteden N, van Tuinen D, Chatagnier O, Elsen A, De Waele D, Panis B, Gianinazzi-Pearson V (2013) Mycorrhiza-induced resistance against the root-knot nematode Meloidogyne incognita involves priming of defense gene responses in tomato. Soil Biology & Biochemistry 60, 45–54.
| Mycorrhiza-induced resistance against the root-knot nematode Meloidogyne incognita involves priming of defense gene responses in tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXktlKgsL0%3D&md5=a5bd8c2f24c7d80fbecbc78e4237531fCAS |
Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Annals of Botany 111, 1021–1058.
| Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXoslWjs7c%3D&md5=afd3f490bfec312a8d1b426d0116872fCAS | 23558912PubMed |
Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Canadian Journal of Botany 82, 1198–1227.
| Prospects and limitations for mycorrhizas in biocontrol of root pathogens.Crossref | GoogleScholarGoogle Scholar |
