Stress Biology in Plants


In our laboratory we investigate the mechanisms of tolerance in plants against adverse environmental situations, including biotic and abiotic stress. These environmental challenges present as a common element the imposition of secondary oxidative stress due to disturbances in redox homeostasis, especially in chloroplasts. With the purpose of trying to restore redox conditions through genetic manipulation of components of the photosynthetic electronic transport chain, we have obtained transgenic plants with multiple tolerance to different sources of environmental stress (drought, salinity, high irradiation, herbicides and pathogenic microorganisms). These plants present alterations in foliar development and senescence.

Research Lines

Development of crops of agronomic relevance (tomato, potato, maize) with higher yield and increased tolerance to environmental stress by genetic manipulation of the redox biochemistry of chloroplasts

Results in model plants indicate that the modification of the redox balance of chloroplasts through alternative electron transports increases tolerance to biotic and abiotic environmental stress, and modifies the architecture of the plant, reducing the vegetative biomass. This project aims to investigate the effect of these interventions on crops of agronomic interest with different photosynthetic mechanisms and exploitation characteristics. It will be studied how the introduction of alternative electron transports in the different types of chloroplasts (mesophyll, vascular sheath) affects the photosynthetic capacity of a C4 plant (maize). Also, the impact of these modifications on the yield of fruits (tomato), tubers (potato) and seeds (maize) will be evaluated.

Modulation of the mitochondrial redox state and its role in stress tolerance and reproduction in plants

The main function of redox processes is to provide energy and reducing power, in addition to generating intermediates that act in signaling networks associated with multiple environmental and morphogenetic responses of plants. Under light conditions, the signals come mainly from the chloroplasts, and although the contribution of mitochondrial redox systems to such processes is less well known than the chloroplast, it has been shown that mitochondria play a relevant role in the response to pathogens and the gametogenesis. In our working group, we have developed gene intervention methods that allow us to alter different oxidation-reduction pathways, and thus predictably modify the levels of redox intermediates, allowing us to study their effect on morphogenesis and tolerance to environmental stress. Although the bulk of the work has focused on chloroplasts, in this project, transgenic plants with alterations in mitochondrial redox pathways are used in order to contribute to the knowledge of these systems. The lines are characterized in terms of tolerance to various sources of abiotic and biotic stress, as well as their yield. The effect of these modifications on processes linked to gametogenesis will be studied, making use of mutants with defects in male and female gametogenesis.

Design of a non-invasive biosensor to detect NADP+/NADPH levels in plant cells

Different intracellular redox changes modulate major transitions in all living organisms, including nutrition, proliferation, defense, senescence, and programmed death. In plants, there are at least three fundamental redox systems: thiol-disulfide, ascorbate and pyridine nucleotides, in addition to the role played by reactive oxygen and nitrogen species. It is therefore of vital importance to have non-invasive methodological tools capable of estimating the levels and redox state of these systems in vivo, as well as determining their spatio-temporal distribution in a dynamic manner. In our group we have developed a biosensor sensitive to the redox state. The genetically encoded probe is specific for NADP(H) and is based on a fusion product between an NADP(H)-dependent enzyme and the coding sequence for the redox state-sensitive fluorescent protein roGFP2. The detection of NADP+/NADPH levels and their redox potential in vivo will make it possible to study the relationship between electronic distribution and stress tolerance, with a view to understanding a fundamental mechanism of biological regulation and manipulating it for agronomic purposes.

Chloroplast redox biochemistry in leaf development

Foliar development constitutes a crucial stage in the growth and reproduction of a plant, since the primary assimilation of carbon takes place in the leaves, which will allow the organism to complete the vegetative development and the maximum production of fruits and seeds. Reactive oxygen species (ROS) contribute at different stages of this process. Photosynthesis directly and indirectly affects the processes of normal growth and development of plants, acclimatization and tolerance to unfavorable environmental conditions and is one of the determinants of productivity. Chloroplasts represent the largest source of light-dependent ROS, and the project is based on the hypothesis that their redox state generates signals that modulate the leaf development program. We use as a tool to modify the chloroplast redox state tobacco and Arabidopsis lines that have altered their photosynthetic electron transport chain (PETC) at different points due to the expression of different cyanobacterial flavoproteins, which remain functional in plants despite their evolutionary divergence. It will be determined how the redox state of chloroplasts influences the size and foliar biomass in these plants, and consequently on the production of fruits and seeds, especially characterizing the contribution of ROS and the redox state of PETC on the different stages of foliar development.

Selected Publications

  • Expression of Flavodiiron Proteins Flv2-Flv4 in Chloroplasts of Arabidopsis and Tobacco Plants Provides Multiple Stress Tolerance. Int J Mol Sci. 22:1178. Vicino P, Carrillo J, Gómez R, Shahinnia F, Tula S, Melzer M, Rutten T, Carrillo N, Hajirezaei MR, Lodeyro AF. (2021)
  • Photosynthetic characterization of flavodoxin-expressing tobacco plants reveals a high light acclimation-like phenotype. Biochim Biophys Acta Bioenerg. 1861:148211. Gómez R, Figueroa N, Melzer M, Hajirezaei MR, Carrillo N, Lodeyro AF. (2020).
  • Transcriptional and Metabolic Profiling of Potato Plants Expressing a Plastid-Targeted Electron Shuttle Reveal Modulation of Genes Associated to Drought Tolerance by Chloroplast Redox Poise. Int J Mol Sci. 21:7199. Karlusich JJP, Arce RC, Shahinnia F, Sonnewald S, Sonnewald U, Zurbriggen MD, Hajirezaei MR, Carrillo N. (2020).
  • Expression of a Chloroplast-Targeted Cyanobacterial Flavodoxin in Tomato Plants Increases Harvest Index by Altering Plant Size and Productivity. Front. Plant Sci. 10:1432. Mayta ML, Arce RC, Zurbriggen MD, Valle EM, Hajirezaei MR, Zanor MI, Carrillo N. (2019)
  • Expression of a Plastid-Targeted Flavodoxin Decreases Chloroplast Reactive Oxygen Species Accumulation and Delays Senescence in Aging Tobacco Leaves. Front. Plant Sci. 9:1039. Mayta ML, Lodeyro AF, Guiamet JJ, Tognetti VB, Melzer M, Hajirezaei MR, Carrillo N. (2018).
  • Faster photosynthetic induction in tobacco by expressing cyanobacterial flavodiiron proteins in chloroplasts. Photosynth. Res. 136:129-138. Gómez R, Carrillo N, Morelli MP, Tula S, Shahinnia F, Hajirezaei MR, Lodeyro AF. (2018).
  • Reactive oxygen species generated in chloroplasts contribute to tobacco leaf infection by the necrotrophic fungus Botrytis cinerea. Plant J. 92:761-773. Rossi FR, Krapp AR, Bisaro F, Maiale SJ, Pieckenstain FL, Carrillo N. (2017).
  • Chloroplast Redox Status Modulates Genome-Wide Plant Responses during the Non-host Interaction of Tobacco with the Hemibiotrophic Bacterium Xanthomonas campestris pv. vesicatoria. Front. Plant Sci. 8:1158. Pierella Karlusich JJ, Zurbriggen MD, Shahinnia F, Sonnewald S, Sonnewald U, Hosseini SA, Hajirezaei MR, Carrillo N. (2017).
  • Suppression of Reactive Oxygen Species Accumulation in Chloroplasts Prevents Leaf Damage but Not Growth Arrest in Salt-Stressed Tobacco Plants. PLoS One. 11:e0159588. Lodeyro AF, Giró M, Poli HO, Bettucci G, Cortadi A, Ferri AM, Carrillo N. (2016)
  • Flavodoxin displays dose-dependent effects on photosynthesis and stress tolerance when expressed in transgenic tobacco plants. Planta. 236:1447-58. Ceccoli RD, Blanco NE, Segretin ME, Melzer M, Hanke GT, Scheibe R, Hajirezaei MR, Bravo-Almonacid FF, Carrillo N. (2012)

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  • Stress tolerant plants. Carrillo, N., Giró, M., Lodeyro, A.F., Zurbriggen, M.D. (2010), US patent WO2011/018662 A1.
  • Un método para el control de malezas en cultivos vegetales. Ceccarelli, E.A., Sosa, G., Carrillo, N., Useglio, M., Lagorio, S. (2008) Argentina Nº de registro: 80101113.
  • Stress tolerant plants. Tognetti, V., Palatnik, J., Fillat, M., Valle, E., Carrillo, N. (2002). EU patent Nº 02801941.2-2405-GB0204612.
  • Stress tolerant plants. Palatnik, J., Fillat, M., Carrillo, N., Valle, E., Tognetti, V. (2004) US patent Nº 6,781,034 B2.