ADAPTIVE GENETICS AND GENOMICS

Group leader: Jose María Jiménez Gómez - Researcher CSIC-INIA
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Personnel:


 

Research overview:

Since their appearance on earth, plants have naturally evolved mechanisms to thrive in every possible ecosystem. Some of the most interesting cases of plant adaptation have occurred during domestication, where humans strongly selected for characteristics of agricultural interest. Understanding the molecular basis of these adaptive mechanisms is one of the mayor quests in modern biology and the goal of the Adaptive Genomics and Genetics group. We believe that knowledge on the genes and proteins responsible for the variation we observe in the world today will help us breed better crops in the future.

The Adaptive Genomics and Genetics group combines expertise in genomics, genetics and molecular biology and works mainly in two model systems: Arabidopsis thaliana and tomato. Arabidopsis is our model to study natural adaptation, because of its worldwide distribution across many different environments, its small genome, ease of growth and its abundant genetic and genomic resources. Tomato is our model for domestication because its importance as food, its relatively small homozygous genome, and its well-studied domestication history.


Research lines:


Circadian rhythms in agriculture


Our lab showed that domestication delayed circadian rhythms in tomato through selection of knockout alleles of EID1 and LNK2, two light signaling genes (Figure 1). Our working hypothesis is that this modification of light signaling and circadian rhythms represent an advantage for tomato under the long days it encountered when it moved out of its equatorial origin. Our lab works now towards demonstrating this hypothesis and towards characterizing the relationship between light signaling, circadian rhythms and plant performance.


Figure 1. Domestication delayed circadian rhythms in tomato. A) Mean relative position of cotyledon tip over time under constant light of 34 cultivated tomato accessions (red) and 44 S. pimpinellifolium accessions (yellow). Colored shading shows SEM; hatched areas in the background indicate subjective nights. Data from 8 independent experiments. B) Mean circadian period and phase estimates ± SEM (n = 2-5) of the genotypes shown in A). C) Genome-wide logarithm of the odds (LOD) scores from a QTL analysis on leaf movements for phase (red ) and period (black) in a S. pimpinellifolium x S. lycopersicum RIL population. The dashed horizontal line indicates the 5 % significance threshold. D) Mean period (left) and phase (right) estimates ± SEM of transgenic lines carrying wild (yellow) or cultivated (red) alleles of LNK2 (left) and EID1 (right). Stars indicate significant differences (one-way ANOVA and post-hoc Tukey’s HSD test, p < 0.01). E) Gene model representations for EID1 and LNK2 indicating the mutations found in cultivated tomato. F) frequency of mutations in EID1 and LNK2 shown in E) among accessions representing several domestication steps from left to right. Number of accessions of each group is indicated on the x axis.
 


Genomics of tomato domestication


Large sets of genomic resources such as resequencing, metabolomics and transcriptomics for cultivated and wild tomato accessions have been made publicly available in the last years (Figure 2). Our lab is using these datasets to investigate the effects of domestication and breeding in the genome of this crop. For example, we collaborate with other groups to study the evolution of transposable elements along tomato domestication or the effect of wild introgressions in the genome of cultivated tomato.


Figure 2. Tomato phylogeny. Neighbor-joining tree of tomato accessions constructed from ~1800 genome-wide SNPs extracted from short read (~700 accessions) and microarray data (~1000 accessions). Color in each accession is determined by its passport data (gold color for accessions of unknown origin). Outside circles were drawn to delimit sensible phylogenetic groups.
 


Arabidopsis natural variation


We have been exploring natural variation in metabolite content and gene expression in Arabidopsis thaliana. This is allowing us to find genes and mutations that change the chemical composition or the regulatory networks of plants adapted to different environments. The figure below shows QTL peaks for 22 metabolites that show variation in a Col x Cvi recombinant inbred line population.


Figure 3. Metabolite QTLs in Arabidopsis. Heatmap of logarithm of the odds (LOD) scores scores from QTL analysis on 22 metabolites that present variation in a Col-0 x Cvi recombinant inbred line population. Plants were grown in two independent experiments in 4 different conditions (represented by colored circles on the y axis). Black lines indicate the highest LOD score for each metabolite and condition.
 

 

 


Representative Publications

Xue, Z., Ferrand, M., Gilbault, E., Zurfluh, O., Clément, G., Marmagne, A., Huguet, S., Jiménez-Gómez, J.M., Krapp, A., Meyer, C., Loudet, O. 2024. Natural variation in response to combined water and nitrogen deficiencies in Arabidopsis. The Plant Cell koae173. DOI: 10.1093/plcell/koae173

Pérez-Alfocea, F., Borghi, M., Guerrero, J.J., Jiménez, A.R., Jiménez-Gómez, J.M., Fernie, A.R., Bartomeus, I. 2024. Pollinator-assisted plant phenotyping, selection, and breeding for crop resilience to abiotic stresses. The Plant Journal. DOI: 10.1111/tpj.16748

Domínguez, M., Dugas, E., Benchouaia, M., Leduque, B., Jiménez-Gómez, J.M., Colot, V., Quadrana, L. 2020. The impact of transposable elements on tomato diversity. Nature Communications 11, 4058. DOI: 10.1038/s41467-020-17874-2

Zhang, L., Jiménez-Gómez, J.M. 2020. Functional analysis of FRIGIDA using naturally occurring variation in Arabidopsis thaliana. The Plant Journal 103, 154–165. DOI: 10.1111/tpj.14716

Van Dooren, T.J.M., Silveira, A.B., Gilbault, E., Jiménez-Gómez, J.M., Martin, A., Bach, L., Tisné, S., Quadrana, L., Loudet, O., Colot, V. 2020. Mild drought in the vegetative stage induces phenotypic, gene expression, and DNA methylation plasticity in Arabidopsis but no transgenerational effects. Journal of Experimental Botany 71, 3588–3602. DOI: 10.1093/jxb/eraa132

Yuste-Lisbona, F.J., Fernández-Lozano, A., Pineda, B., Bretones, S., Ortíz-Atienza, A., García-Sogo, B., Müller, N.A., Angosto, T., Capel, J., Moreno, V., Jiménez-Gómez, J.M., Lozano, R. 2020. ENO regulates tomato fruit size through the floral meristem development network. Proceedings of the National Academy of Sciences 117, 8187–8195. DOI: 10.1073/pnas.1913688117

Hu, Y., Mesihovic, A., Jiménez-Gómez, J.M., Röth, S., Gebhardt, P., Bublak, D., Bovy, A., Scharf, K.-D., Schleiff, E., Fragkostefanakis, S. 2020. Natural variation in HsfA2 pre-mRNA splicing is associated with changes in thermotolerance during tomato domestication. New Phytologist 225, 1297–1310. DOI: 10.1111/nph.16221

Huertas, R., Catalá, R., Jiménez-Gómez, J.M., Mar Castellano, M., Crevillén, P., Piñeiro, M., Jarillo, J.A., Salinas, J. 2019. Arabidopsis SME1 Regulates Plant Development and Response to Abiotic Stress by Determining Spliceosome Activity Specificity. The Plant Cell 31, 537–554. DOI: 10.1105/tpc.18.00689

Fantini, E., Sulli, M., Zhang, L., Aprea, G., Jiménez-Gómez, J.M., Bendahmane, A., Perrotta, G., Giuliano, G., Facella, P. 2019. Pivotal Roles of Cryptochromes 1a and 2 in Tomato Development and Physiology. Plant Physiology 179, 732–748. DOI: 10.1104/pp.18.00793

Albert, E., Duboscq, R., Latreille, M., Santoni, S., Beukers, M., Bouchet, J.-P., Bitton, F., Gricourt, J., Poncet, C., Gautier, V., Jiménez-Gómez, J.M., Rigaill, G., Causse, M. 2018. Allele-specific expression and genetic determinants of transcriptomic variations in response to mild water deficit in tomato. The Plant Journal 96, 635–650. DOI: 10.1111/tpj.14057

Olate, E., Jiménez-Gómez, J.M., Holuigue, L., Salinas, J. 2018. NPR1 mediates a novel regulatory pathway in cold acclimation by interacting with HSFA1 factors. Nature Plants 4, 811–823. DOI: 10.1038/s41477-018-0254-2

Müller, N.A., Zhang, L., Koornneef, M., Jiménez-Gómez, J.M. 2018. Mutations in EID1 and LNK2 caused light-conditional clock deceleration during tomato domestication. Proceedings of the National Academy of Sciences 115, 7135–7140. DOI: 10.1073/pnas.1801862115

Ashoub, A., Müller, N., Jiménez-Gómez, J.M., Brüggemann, W. 2018. Prominent alterations of wild barley leaf transcriptome in response to individual and combined drought acclimation and heat shock conditions. Physiologia Plantarum 163, 18–29. DOI: 10.1111/ppl.12667

Magnani, E., Jiménez-Gómez, J.M., Soubigou-Taconnat, L., Lepiniec, L., Fiume, E. 2017. Profiling the onset of somatic embryogenesis in Arabidopsis. BMC Genomics 18, 998. DOI: 10.1186/s12864-017-4391-1

Serin, E.A.R., Snoek, L.B., Nijveen, H., Willems, L.A.J., Jiménez-Gómez, J.M., Hilhorst, H.W.M., Ligterink, W. 2017. Construction of a High-Density Genetic Map from RNA-Seq Data for an Arabidopsis Bay-0 × Shahdara RIL Population. Frontiers in Genetics 8, 201. DOI: 10.3389/fgene.2017.00201

Álvarez, M.F., Angarita, M., Delgado, M.C., García, C., Jiménez-Gomez, J., Gebhardt, C., Mosquera, T. 2017. Identification of Novel Associations of Candidate Genes with Resistance to Late Blight in Solanum tuberosum Group Phureja. Frontiers in Plant Science 8, 1040. DOI: 10.3389/fpls.2017.01040

Balcke, G.U., Bennewitz, S., Bergau, N., Athmer, B., Henning, A., Majovsky, P., Jiménez-Gómez, J.M., Hoehenwarter, W., Tissier, A. 2017. Multi-Omics of Tomato Glandular Trichomes Reveals Distinct Features of Central Carbon Metabolism Supporting High Productivity of Specialized Metabolites. The Plant Cell 29, 960–983. DOI: 10.1105/tpc.17.00060

Costa, M.-C.D., Artur, M.A.S., Maia, J., Jonkheer, E., Derks, M.F.L., Nijveen, H., Williams, B., Mundree, S.G., Jiménez-Gómez, J.M., Hesselink, T., Schijlen, E.G.W.M., Ligterink, W., Oliver, M.J., Farrant, J.M., Hilhorst, H.W.M. 2017. A footprint of desiccation tolerance in the genome of Xerophyta viscosa. Nature Plants 3, 1–10. DOI: 10.1038/nplants.2017.38

Soyk, S., Müller, N.A., Park, S.J., Schmalenbach, I., Jiang, K., Hayama, R., Zhang, L., Van Eck, J., Jiménez-Gómez, J.M., Lippman, Z.B. 2017. Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato. Nature Genetics 49, 162–168. DOI: 10.1038/ng.3733

Srinivasan, A., Jiménez-Gómez, J.M., Fornara, F., Soppe, W.J.J., Brambilla, V. 2016. Alternative splicing enhances transcriptome complexity in desiccating seeds. Journal of Integrative Plant Biology 58, 947–958. DOI: 10.1111/jipb.12482

Bar, M., Israeli, A., Levy, M., Ben Gera, H., Jiménez-Gómez, J.M., Kouril, S., Tarkowski, P., Ori, N. 2016. CLAUSA Is a MYB Transcription Factor That Promotes Leaf Differentiation by Attenuating Cytokinin Signaling. The Plant Cell 28, 1602–1615. DOI: 10.1105/tpc.16.00211

Mosquera, T., Alvarez, M.F., Jiménez-Gómez, J.M., Muktar, M.S., Paulo, M.J., Steinemann, S., Li, J., Draffehn, A., Hofmann, A., Lübeck, J., Strahwald, J., Tacke, E., Hofferbert, H.-R., Walkemeier, B., Gebhardt, C. 2016. Targeted and Untargeted Approaches Unravel Novel Candidate Genes and Diagnostic SNPs for Quantitative Resistance of the Potato (Solanum tuberosum L.) to Phytophthora infestans Causing the Late Blight Disease. PLOS ONE 11, e0156254. DOI: 10.1371/journal.pone.0156254

Müller, N.A., Wijnen, C.L., Srinivasan, A., Ryngajllo, M., Ofner, I., Lin, T., Ranjan, A., West, D., Maloof, J.N., Sinha, N.R., Huang, S., Zamir, D., Jiménez-Gómez, J.M. 2016. Domestication selected for deceleration of the circadian clock in cultivated tomato. Nature Genetics 48, 89–93. DOI: 10.1038/ng.3447

Perea-Resa, C., Carrasco-López, C., Catalá, R., Turečková, V., Novak, O., Zhang, W., Sieburth, L., Jiménez-Gómez, J.M., Salinas, J. 2016. The LSM1-7 Complex Differentially Regulates Arabidopsis Tolerance to Abiotic Stress Conditions by Promoting Selective mRNA Decapping. The Plant Cell 28, 505–520. DOI: 10.1105/tpc.15.00867

Schmalenbach, I., Zhang, L., Reymond, M., Jiménez-Gómez, J.M. 2014. The relationship between flowering time and growth responses to drought in the Arabidopsis Landsberg erecta x Antwerp-1 population. Frontiers in Plant Science 5, 609. DOI: 10.3389/fpls.2014.00609

Gloggnitzer, J., Akimcheva, S., Srinivasan, A., Kusenda, B., Riehs, N., Stampfl, H., Bautor, J., Dekrout, B., Jonak, C., Jiménez-Gómez, J.M., Parker, J.E., Riha, K. 2014. Nonsense-Mediated mRNA Decay Modulates Immune Receptor Levels to Regulate Plant Antibacterial Defense. Cell Host & Microbe 16, 376–390. DOI: 10.1016/j.chom.2014.08.010

Schmalenbach, I., Zhang, L., Ryngajllo, M., Jiménez-Gómez, J.M. 2014. Functional analysis of the Landsberg erecta allele of FRIGIDA. BMC Plant Biology 14, 218. DOI: 10.1186/s12870-014-0218-2

Bolger, A., Scossa, F., Bolger, M.E., Lanz, C., Maumus, F., Tohge, T., Quesneville, H., Alseekh, S., Sørensen, I., Lichtenstein, G., Fich, E.A., Conte, M., Keller, H., Schneeberger, K., Schwacke, R., Ofner, I., Vrebalov, J., Xu, Y., Osorio, S., Aflitos, S.A., Schijlen, E., Jiménez-Goméz, J.M., Ryngajllo, M., Kimura, S., Kumar, R., Koenig, D., Headland, L.R., Maloof, J.N., Sinha, N., van Ham, R.C.H.J., Lankhorst, R.K., Mao, L., Vogel, A., Arsova, B., Panstruga, R., Fei, Z., Rose, J.K.C., Zamir, D., Carrari, F., Giovannoni, J.J., Weigel, D., Usadel, B., Fernie, A.R. 2014. The genome of the stress-tolerant wild tomato species Solanum pennellii. Nature Genetics 46, 1034–1038. DOI: 10.1038/ng.3046

Koenig, D., Jiménez-Gómez, J.M., Kimura, S., Fulop, D., Chitwood, D.H., Headland, L.R., Kumar, R., Covington, M.F., Devisetty, U.K., Tat, A.V., Tohge, T., Bolger, A., Schneeberger, K., Ossowski, S., Lanz, C., Xiong, G., Taylor-Teeples, M., Brady, S.M., Pauly, M., Weigel, D., Usadel, B., Fernie, A.R., Peng, J., Sinha, N.R., Maloof, J.N. 2013. Comparative transcriptomics reveals patterns of selection in domesticated and wild tomato. Proceedings of the National Academy of Sciences 110, E2655–E2662. DOI: 10.1073/pnas.1309606110

Sharlach, M., Dahlbeck, D., Liu, L., Chiu, J., Jiménez-Gómez, J.M., Kimura, S., Koenig, D., Maloof, J.N., Sinha, N., Minsavage, G.V., Jones, J.B., Stall, R.E., Staskawicz, B.J. 2013. Fine genetic mapping of RXopJ4, a bacterial spot disease resistance locus from Solanum pennellii LA716. Theoretical and Applied Genetics 126, 601–609. DOI: 10.1007/s00122-012-2004-6

Chitwood, D.H., Kumar, R., Headland, L.R., Ranjan, A., Covington, M.F., Ichihashi, Y., Fulop, D., Jiménez-Gómez, J.M., Peng, J., Maloof, J.N., Sinha, N.R. 2013. A Quantitative Genetic Basis for Leaf Morphology in a Set of Precisely Defined Tomato Introgression Lines. The Plant Cell 25, 2465–2481. DOI: 10.1105/tpc.113.112391

Chitwood, D.H., Headland, L.R., Filiault, D.L., Kumar, R., Jiménez-Gómez, J.M., Schrager, A.V., Park, D.S., Peng, J., Sinha, N.R., Maloof, J.N. 2012. Native Environment Modulates Leaf Size and Response to Simulated Foliar Shade across Wild Tomato Species. PLOS ONE 7, e29570. DOI: 10.1371/journal.pone.0029570

Jiménez-Gómez, J.M., Wallace, A.D., Maloof, J.N. 2010. Network Analysis Identifies ELF3 as a QTL for the Shade Avoidance Response in Arabidopsis. PLOS Genetics 6, e1001100. DOI: 10.1371/journal.pgen.1001100