Genetics and Epigenetics of Plant Abiotic Stress Response and Resilience

Towards the development of abiotic stress resilient crops

The Michal Lieberman-Lazarovich Lab

Scientific overviewScientific overview
In an era of global warming, increasing episodes of weather extremes and population growth, the issue of food security is of top importance. Among the various effects of climate change, elevated temperatures are a major threat to crop productivity. Current adaptations to high temperatures via agricultural management systems are insufficient to sustain yield, therefore breeding for heat tolerant crops is crucial. We aim at improving reproductive stress tolerance in Solanaceous crops, focusing on heat-stress tolerance in tomato, one of the most important vegetable crops worldwide.

In order to promote the development of stress resilient cultivars, our overall aim is to understand plants’ responses to abiotic stresses. We utilize various genotypes and cultivars, test them under different environmental conditions and combination of stresses, and perform physiological and molecular assays to characterize the response. We pursue the genetic and epigenetic elements that are involved in stress response and tolerance. In alignment with this aim, we are part of the COST action CA19125-Epi-Catch (EPIgenetic mechanisms of Crop Adaptation To Climate cHange). Visit our websites for further information and activities (https://61e6e24bcea16.site123.me/).

Our lab is part of the Department of Vegetables and Field Crops Research in the Plant Sciences Institute, at the Agricultural Research Organization (ARO) – Volcani Center.

Heat-stress tolerance in processing tomato varieties

This projects targets genetic diversity between tomato cultivars that differ in their capability to set fruit under high temperatures. By performing detailed developmental, physiological and molecular characterization of the plants under field as well as controlled stress conditions, we aim at identifying the array of traits and genes that underlie heat-tolerance in processing tomato.

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Abiotic stress tolerance in wild tomato species

This project involves screening a population of introgression lines of wild species into cultivated tomato. Under the hypothesis that wild relatives of the cultivated tomato evolved in harsh environments and have evolved to cope well with abiotic stress conditions, we will screen the introgression population under heat stress conditions in order to identify QTL and genes related to heat stress tolerance.

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Secondary metabolites as stress-relief agents

In this project, we test the hypothesis that particular naturally occurring secondary metabolites have the capacity to reduce stress-induced damage due to their antioxidative capacity. We focus on pollen viability measurements under stress and non-stress conditions, in tomato mutants with altered levels of secondary metabolites in pollen.

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DNA methylation in the heat-stress response in tomato

Recent advances in the field of epigenetics have revealed a plethora of gene control mechanisms that mediate plant's response to its environment, and could contribute to phenotypic variation. Direct intervention of epigenetic control systems hold the enticing promise of creating new sources of variability that could enhance crop performance. We investigate the involvement of DNA methylation in the epigenetic regulation of heat stress response in tomato.

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Michal Lieberman Lazarovich, PhD

Principal investigator

Golan Miller, PhD

Lab manager

Pawan Kumar, PhD

Post-doctoral fellow

Liron Ezra

MSc student

Tal Gurevich

MSc. student

Guy Barzilay

MSc. student

Sarit Vilenchink

Undergraduate student

Mushka Landa

Greenhouse manager

Tzion Doitch-Movshovich

Undergraduate student

Rotem Zelingher

Intern

Geki Shoef

Undergraduate student

Fengde Wang, PhD

Visiting scientist

Etel Motenko

Undergraduate student

Avital Beery

Lab technician

Prashant Kumar Singh, PhD

Postdoctoral fellow

Neta Bashary

MSc. student

RESEARCH ARTICLES

Rutley, N., Miller, G., Wang, F., Harper, J. F., Miller, G., and Lieberman-Lazarovich, M. (2021). Enhanced Reproductive Thermotolerance of the Tomato high pigment 2 Mutant is Associated with Increased Accumulation of Flavonols in Pollen. Front. Plant Sci. 12, 672368. doi:10.3389/fpls.2021.672368.

Miller, G., Beery, A., Singh, P. K., Wang, F., Zelingher, R., Motenko, E., and Lieberman-Lazarovich, M. (2021). Contrasting Processing Tomato Cultivars Unlink Yield and Pollen Viability Under Heat Stress. AoB Plants 13. doi:10.1093/aobpla/plab046.

Singh, P. K., Miller, G., Faigenboim, A., and Lieberman-lazarovich, M. (2021). The Tomato ddm1b Mutant Shows Decreased Sensitivity to Heat Stress Accompanied by Transcriptional Alterations. Genes (Basel). 1–9. https://doi.org/10.3390/genes12091337.

Lieberman-Lazarovich, M., Yahav, C., Israeli, A., and Efroni, I. (2019). Deep Conservation of cis-Element Variants Regulating Plant Hormonal Responses. Plant Cell 31, 2559–2572. doi:10.1105/tpc.19.00129.

Catoni, M., Griffiths, J., Becker, C., Zabet, N. R., Bayon, C., Dapp, M., Lieberman-Lazarovich, M., Weigel, D., and Paszkowski, J. (2017). DNA Sequence Properties That Predict Susceptibility to Epiallelic Switching. EMBO J. 36, 617–628. doi:10.15252/embj.201695602.

Lieberman-Lazarovich, M., Melamed-Bessudo, C., De Pater, S., and Levy, A. A. (2013). Epigenetic Alterations at Genomic Loci Modified by Gene Targeting in Arabidopsis thaliana. PLoS One 8, e85383. doi:10.1371/journal.pone.0085383.

Mirouze, M*., Lieberman-Lazarovich, M*., Aversano, R., Bucher, E., Nicolet, J., Reinders, J., and Paszkowski, J. (2012). Loss of DNA Methylation Affects The Recombination Landscape in Arabidopsis. Proc. Natl. Acad. Sci. 109, 5880–5885. *equal contribution https://doi.org/10.1073/pnas.1120841109

Bino, R.J., De Vos, C.H.R., Lieberman, M., Hall, R.D., Bovy, A., Jonker, H.H., Tikunov, Y., Lommen, A., Moco, S. and Levin, I. (2005). The Light-hyperresponsive high pigment-2dg Mutation of Tomato: Alterations in The Fruit Metabolome. New Phytol. 166, 427–438. https://doi.org/10.1111/j.1469-8137.2005.01362.x.

Lieberman, M., Segev, O., Gilboa, N. Lalazar, A., and Levin, I. (2004). The Tomato Homolog of The Gene Encoding UV-Damaged DNA Binding Protein 1 (DDB1) Underlined as the Gene That Causes the high pigment-1 Mutant Phenotype. Theor. Appl. Genet. 108, 1574–1581. https://doi.org/10.1007/s00122-004-1584-1

REVIEW PAPERS

Guarino, F., Cicatelli, A., Castiglione, S., Agius, D. R., Orhun, G. E., Fragkostefanakis, S., Leclercq, J., Dobránszki, J., Kaiserli, E., Lieberman-Lazarovich, M., Sõmera, M., Sarmiento, C., Vettori, C., Paffetti, D., Poma, A., Moschou, P. N., Gašparović, M., Yousefi, S., Vergata, C., Berger, M., Gallusci, P., Miladinović, D., and Martinelli, F. (2022). An Epigenetic Alphabet of Crop Adaptation to Climate Change. Front. Genet. 13, 818727. https://doi.org/10.3389/fgene.2022.818727

Kakoulidou, I., Avramidou, E. V, Baránek, M., Brunel-Muguet, S., Farrona, S., Johannes, F., Kaiserli, E., Lieberman-Lazarovich, M., Martinelli, F., Mladenov, V., Testillano, P. S., Vassileva, V., Maury, S. (2021). Epigenetics for Crop Improvement in Times of Global Change. Biology (Basel). 10, 766. https://doi.org/10.3390/biology10080766.

Levin, I., de Vos, C. R., Tadmor, Y., Bovy, A., Lieberman, M., Oren-Shamir, M., Segev, O., Kolotilin, I., Keller, M., Ovadia, R., Meir, A., and Bino, R. J. (2006). High pigment tomato mutants—more than just lycopene (a review). Isr. J. Plant Sci. 54(3), 179-190. https://brill.com/view/journals/ijps/54/3/article-p179_4.xml
 
BOOK CHAPTERS


Lieberman-Lazarovich, M., Kim, T., Singh, P. K., and Begcy, K. (2021). “Chapter 6 - Epigenetics in horticultural crops: consequences and applications in abiotic stress tolerance,” in Stress Tolerance in Horticultural Crops Challenges and Mitigation Strategies, eds. A. Chandra Rai, A. Rai,
K. Kumar Rai, V. P. Rai, and A. B. T.-S. T. in H. C. Kumar (Woodhead Publishing), 75–90. https://doi.org/10.1016/B978-0-12-822849-4.00016-4.

Lieberman-Lazarovich, M., Levy, A.A. (2011). Homologous Recombination in Plants: An Antireview. In: Birchler, J. (eds) Plant Chromosome Engineering. Methods in Molecular Biology, vol 701. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-61737-957-4_3

REGISTERED PATENTS

Brog, Y. M., WOLFENSON, Y. G., Goren, S. Z., Hilman, D., Karchi, H., Lieberman-lazarovich, M., et al. (2020). Plant traits conferred by isolated polynucleotides and polypeptides.

Levin, I., Lieberman, M., Segev, O. A., Gilboa, N., and Lalazar, A. (2013). Isolated nucleotide sequences responsible for the tomato high pigment-1 mutant phenotype (hp-1) and uses thereof.
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