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Arbuscular Mycorrhizal Symbiosis-Induced Expression Changes in Solanum lycopersicum Leaves Revealed by RNA-seq Analysis

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Abstract

Arbuscular mycorrhizal symbiosis is a beneficial association between plant roots and fungi that occurs in approximately 80 % of terrestrial plants and which confers different benefits including mineral nutrient acquisition and enhanced defense capacity. Although mycorrhizal colonization takes place in roots, the symbiosis establishment has systemic effects in other parts of the plant, in processes such as nutrient translocation and systemic resistance. In order to understand the transcriptional changes that occur in leaves of mycorrhizal plants, we used RNA-seq technology to obtain the transcriptomes of leaves from mycorrhizal and non-mycorrhizal tomato plants (Solanum lycopersicum). Four weeks after inoculation with the fungus Rhizophagus irregularis, leaves from mycorrhizal and non-mycorrhizal tomato plants were used for transcriptome sequencing. Of the 21,113 genes expressed in tomato leaves, 742 genes displayed differential expression between the mycorrhizal and non-mycorrhizal conditions. Most of the transcriptional changes occurred in the “protein,” “RNA,” “signaling,” “transport,” “biotic and abiotic stresses,” and “hormone metabolism” categories. Some transcriptional changes also occurred in P, N, and sugar transporters, as would be expected for mycorrhizal colonization. Finally, several differentially expressed genes may be related to systemic defense priming, in agreement with our demonstration that symbiotic plants exhibited mycorrhiza-induced resistance against the foliar pathogen Xanthomonas campestris pv. vesicatoria. This is the first study to take on a genome-wide analysis aimed at understanding the expression changes in leaves of mycorrhiza-colonized plants. The results will therefore be valuable to future analyses focused on specific genes, as well as detailed studies of the expression profiles of certain gene families.

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Acknowledgments

MLM acknowledges support from CONACyT (project no. 102237) and SIP-IPN (project no. 20131537) grants. RGCG acknowledges CONACyT (219635) and PIFI-IPN graduate fellowships. The authors thank Dr. Dagoberto Armenta for his assistance with the statistical analyses and Brandon Loveall of Improvence for English proofreading of the manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

Author contributions

RGCG participated in the experimental design, performed most of the experiments, participated in the sequencing analysis, and drafted the manuscript. MABI, ACM, and CLCV participated in the sequence analysis and drafted the manuscript. CMRD, IEMM, and MAVL participated in the experimental design and drafted the manuscript. AVO assisted in drafting the manuscript. MLM conceived the study and participated in its design and coordination, as well as the manuscript writing. All authors read and approved the final manuscript.

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Authors and Affiliations

  1. Departamento de Biotecnología Agrícola, Instituto Politécnico Nacional CIIDIR-Sinaloa, Blvd. Juan de Dios Bátiz Paredes 250, Guasave, Sinaloa, México

    Rocío Guadalupe Cervantes-Gámez, Mario Alonso Bueno-Ibarra, Carlos Ligné Calderón-Vázquez, Claudia María Ramírez-Douriet, Ignacio Eduardo Maldonado-Mendoza & Melina López-Meyer

  2. Facultad de Ciencias Químico-Biológicas, Universidad Autónoma de Sinaloa, Av. de las Américas y Josefa Ortiz S/N, Culiacán, Sinaloa, México

    Abraham Cruz-Mendívil & Ángel Valdez-Ortíz

  3. Instituto Politécnico Nacional CIBA-Tlaxcala, Ex-Hacienda San Juan Molino Carretera estatal Tecuexcomac-Tepetitla Km 1.5, Tlaxcala, México

    Miguel Ángel Villalobos-López

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  1. Rocío Guadalupe Cervantes-Gámez
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  2. Mario Alonso Bueno-Ibarra
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  3. Abraham Cruz-Mendívil
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  6. Ignacio Eduardo Maldonado-Mendoza
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  7. Miguel Ángel Villalobos-López
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  8. Ángel Valdez-Ortíz
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  9. Melina López-Meyer
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Correspondence to Melina López-Meyer.

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Supplementary Table 1

Primers used in q-PCR to validate RNA-seq results (XLS 34 kb)

Supplementary Table 2

Functional classification of significant differentially expressed mycorrhiza-responsive genes in leaves of tomato plants, according to RNA-seq fold changes (XLS 145 kb)

Supplementary Table 3

Mycorrhiza-responsive genes with significant different expression but less than 10 unique gene reads in one or both treatments (XLS 84 kb)

Supplementary Table 4

Mycorrhiza-responsive genes involved in more than one biological process according to MAPMAN classification (XLS 34 kb)

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Cervantes-Gámez, R.G., Bueno-Ibarra, M.A., Cruz-Mendívil, A. et al. Arbuscular Mycorrhizal Symbiosis-Induced Expression Changes in Solanum lycopersicum Leaves Revealed by RNA-seq Analysis. Plant Mol Biol Rep 34, 89–102 (2016). https://doi.org/10.1007/s11105-015-0903-9

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