GRUPO: Estrés AbiótiKo-Transporte de Potasio en Estrés Abiótico en Plantas y Levaduras

GENERAL DESCRIPTION OF SCIENTIFIC INTERESTS:

Ion homeostasis is a dynamic process and a fundamental requirement for all organisms. Many different minerals are required for essential biochemical processes, but accumulation of these elements is toxic. Thus, all living organisms have developed efficient systems to acquire and store these elements and robust mechanisms to maintain homeostatic concentrations to avoid toxicity and to respond to environmental changes.

Potassium is a key monovalent cation necessary for multiple aspects of cell growth and survival, for example compensation of negative charges of macromolecules, maintenance of electroneutrality, cell turgor and volume, enzyme activity, protein synthesis, and maintenance of proper membrane potential and intracellular pH. The long term, general goal of our research group is to generate new knowledge regarding the regulation of potassium transporters from both plants and yeast which may be applied in future in biotechnological approaches to improve plant drought tolerance and industrial performance of yeast.

CURRENT PROJECTS:

In plants, apart from the basic, general physiological functions listed above for potassium at the cellular level, this cation also plays a key role at the whole plant level, as it is involved in important processes such as stomatal aperture that controls transpirational water loss and plant desiccation. Inward rectifying channels (Kin) are responsible for potassium influx into guard cells and play a key role in stomatal opening. KAT1, and its close homologue KAT2, are the main inward rectifying channels expressed in guard cells. Our current project is focused on the characterization 14 proteins that we have identified in a Split-Ubiquitin protein-protein interaction screen searching for KAT1 potassium channel interactors from the model plant Arabidopsis thaliana.

We are taking several biochemical and genetic approaches to confirm these interactors and their effect on KAT1 activity in plants. The identification of physiologically relevant regulators of K+ channels will aid in the design of approaches that may impact both drought tolerance and pathogen susceptibility, since these pores are responsible for CO2 uptake and transpirational water loss and are the point of entry for certain pathogens.

In addition we are interested in studying the regulation of the high affinity potassium transporter of yeast, Trk1. The regulation of this transporter is crucial for the regulation of nutrient uptake and, recently, a direct effect of both external and internal potassium and pH on ethanol tolerance in conditions relevant for the industrial production of bioethanol has been reported. In addition, several studies clearly indicate that the proteins involved in determining and maintaining plasma membrane potential through the modulation of potassium homeostasis represent promising targets for complimentary antifungal treatments. Therefore, the identification of proteins that regulate the activity of this potassium transporter has potential applications in both agronomic, industrial and medical contexts.

Chevilly S, Dolz-Edo L, Martínez-Sánchez G, Morcillo L, Vilagrosa A, López-Nicolás JM, Blanca J, Yenush L, Mulet JM. (2021)

Distinctive Traits for Drought and Salt Stress Tolerance in Melon (Cucumis melo L.)

Front Plant Sci. 2021 Nov 4;12:777060

Bissoli G, Bono M, Martínez-Almonacid I, Moreno-Peris E, Renard J, Espinosa A, Naranjo MÁ, Yenush L, Fita A, Serrano R, Rodríguez-Burruezo A, Bueso E. (2021)

Seed coat lignification level is crucial in Capsicum spp seed longevity

Physiol Plant. 2021 Nov 19:e13600

Chevilly S, Dolz-Edo L, Morcillo L, Vilagrosa A, López-Nicolás JM, Yenush L, Mulet JM. (2021)

Identification of distinctive physiological and molecular responses to salt stress among tolerant and sensitive cultivars of broccoli (Brassica oleracea var. Italica)

BMC Plant Biol. 2021 Oct 25;21(1):488

Chevilly S, Dolz-Edo L, López-Nicolás JM, Morcillo L, Vilagrosa A, Yenush L, Mulet JM. (2021)

Physiological and Molecular Characterization of the Differential Response of Broccoli (Brassica oleracea var. Italica) Cultivars Reveals Limiting Factors for Broccoli Tolerance to Drought Stress.

J Agric Food Chem. 2021 Sep 8;69(35):10394

Mulet JM, Campos F, Yenush L. (2020)

Ion Homeostasis in Plant Stress and Development

Front Plant Sci. 2020 Nov 20;11:618273

Vazquez-Vilar M, Gandía M, García-Carpintero V, Marqués E, Sarrion-Perdigones A, Yenush L, Polaina J, Manzanares P, Marcos JF, Orzaez D. (2020)

Multigene Engineering by GoldenBraid Cloning: From Plants to Filamentous Fungi and Beyond

Curr Protoc Mol Biol. 2020 Mar;130(1):e116

R Saporta, C Bou, V Frías, JM Mulet (2019)

A Method for a Fast Evaluation of the Biostimulant Potential of Different Natural Extracts for Promoting Growth or Tolerance against Abiotic Stress

Agronomy 9 (3), 143

A Locascio, MC Marques, G García-Martínez, C Corratgé-Faillie (2019)

BCL2-ASSOCIATED ATHANOGENE4 Regulates the KAT1 Potassium Channel and Controls Stomatal Movement

Plant physiology 181 (3), 1277-1294

A Locascio, N Andrés-Colás, JM Mulet, L Yenush (2019)

Saccharomyces cerevisiae as a tool to investigate plant potassium and sodium transporters

International journal of molecular sciences 20 (9), 2133

A Bustamante, MC Marques, A Sanz-Carbonell, JM Mulet, G Gomez (2018)

Alternative processing of its precursor is related to miR319 decreasing in melon plants exposed to cold

Scientific reports 8 (1), 15538

R Porcel, A Bustamante, R Ros, R Serrano, JM Mulet Salort (2018)

BvCOLD1: A novel aquaporin from sugar beet (Beta vulgaris L.) involved in boron homeostasis and abiotic stress

Plant, cell & environment 41 (12), 2844-2857

Hernanz-Koers M, Gandía M, Garrigues S, Manzanares P, Yenush L, Orzaez D, Marcos JF (2018)

FungalBraid: A GoldenBraid-based modular cloning platform for the assembly and exchange of DNA elements tailored to fungal synthetic biology

Fungal Genet Biol;116:51-61

Primo C, Ferri-Blázquez A, Loewith R, Yenush L (2017)

Reciprocal Regulation of Target of Rapamycin Complex 1 and Potassium Accumulation.

The Journal of Biological Chemistry 292: 563-574

Taibi K, del Campo AD, Aguado A, Mulet JM (2016)

Early establishment response of different Pinus nigra ssp salzmanii seed sources on contrasting environments: Implications for future reforestation programs and assisted population migration

Journal of Environmental Management 171: 184-194

Yenush L (2016)

Potassium and Sodium Transport in Yeast

Advances in Experimental Medicine and Biology 892: 187-228

Petrezselyova S, Lopez-Malo M, Canadell D, Roque A, Serra-Cardona A, Marquea MC, Vilaprinyo E, Alves R, Yenush L, Arino J (2016)

Regulation of the Na+/K+-ATPase Ena1 Expression by Calcineurin/Crz1 under High pH Stress: A Quantitative Study

Plos One 11: e0158424

Llopis-Torregrosa V, Ferri-Blazquez A, Adam-Artigues A, Deffontaines E, van Heusden GPH, Yenush L (2016)

Regulation of the Yeast Hxt6 Hexose Transporter by the Rod1 alpha-Arrestin, the Snf1 Protein Kinase, and the Bmh2 14-3-3 Protein.

The Journal of biological chemistry 291: 14973-14985

Marqués MC, Zamarbide-Forés S, Pedelini L, Llopis-Torregrosa V, Yenush L (2015)

A functional Rim101 complex is required for proper accumulation of the Ena1 Na+-ATPase protein in response to salt stress in Saccharomyces cerevisiae

FEMS Yeast Research 15: fov017

Mattiazzi Ušaj M, Prelec M, Brložnik M, Primo C, Curk T, Ščančar J, Yenush L, Petrovič U (2015)

Yeast Saccharomyces cerevisiae adiponectin receptor homolog Izh2 is involved in the regulation of zinc, phospholipid and pH homeostasis

Metallomics 7: 1338-1351

Bueso E, Muñoz-Bertomeu J, Campos F, Brunaud V, Martinez L, Sayas E, Ballester P, Yenush L, Serrano R (2014)

ARABIDOPSIS THALIANA HOMEOBOX 25 uncovers a role for gibberellins in seed longevity

Plant Physiology 164: 999-1010

Ariño J, Aydar E, Drulhe S, Ganser D, Jorrín J, Kahm M, Krause F, Petrezsélyová S, Yenush L, Zimmermannová O, van Heusden GP, Kschischo M, Ludwig J, Palmer C, Ramos J, Sychrová H (2014)

Systems biology of monovalent cation homeostasis in yeast: the translucent contribution

Advances in Microbial Physiology 64: 1-63

Mulet JM, Llopis-Torregrosa V, Primo C, Marqués MC, Yenush L (2013)

Endocytic regulation of alkali metal transport proteins in mammals, yeast and plants

Current Genetics 59: 207-230

Roque E, Serwatowska J, Cruz Rochina M, Wen J, Mysore KS, Yenush L, Beltrán JP, Cañas LA (2013)

Functional specialization of duplicated AP3-like genes in Medicago truncatula

Plant Journal 73: 663-675

Sainz M, Pérez-Rontomé C, Ramos J, Mulet JM, James EK, Bhattacharjee U, Petrich JW, Becana M (2013)

Plant hemoglobins may be maintained in functional form by reduced flavins in the nuclei, and confer differential tolerance to nitro-oxidative stress

Plant Journal 76: 875-887

Ríos G, Cabedo M, Rull B, Yenush L, Serrano R, Mulet JM (2013)

Role of the yeast multidrug transporter Qdr2 in cation homeostasis and the oxidative stress response

FEMS Yeast Research 13: 97-106

Bissoli G, Niñoles R, Fresquet S, Palombieri S, Bueso E, Rubio L, García-Sánchez MJ, Fernández JA, Mulet JM, Serrano R (2012)

Peptidyl-prolyl cis-trans isomerase ROF2 modulates intracellular pH homeostasis in Arabidopsis

Plant Journal 70: 704-716

Kahm M, Navarrete C, Llopis-Torregrosa V, Herrera R, Barreto L, Yenush L, Ariño J, Ramos J, Kschischo M (2012)

Potassium starvation in yeast: mechanisms of homeostasis revealed by mathematical modeling

PLoS Computational Biology 8: e1002548

Barreto L, Canadell D, Petrezselyova S, Navarrete C, Maresova L, Perez-Valle J, Herrera R, Olier I, Giraldo J, Sychrova H, Yenush L, Ramos J, Arino J (2011)

A genomewide screen for tolerance to cationic drugs reveals genes important for potassium homeostasis in Saccharomyces cerevisiae

Eukaryotic Cell 10: 1241-1250

Merchan S, Pedelini L, Hueso G, Calzada A, Serrano R, Yenush L (2011)

Genetic alterations leading to increases in internal potassium concentrations are detrimental for DNA integrity in Saccharomyces cerevisiae

Genes to Cells 16: 152-65

Mulet JM (2011)

Letter to the editor regarding the article by Paganelli et al.

Chemical Research in Toxicology 24: 609

Casado C, Yenush L, Melero C, Ruiz Mdel C, Serrano R, Pérez-Valle J, Ariño J, Ramos J (2010)

Regulation of Trk-dependent potassium transport by the calcineurin pathway involves the Hal5 kinase

FEBS Letters 584: 2415-2420

Pérez-Valle J, Rothe J, Primo C, Martínez Pastor M, Ariño J, Pascual-Ahuir A, Mulet JM, Serrano R, Yenush L (2010)

The Hal4 and Hal5 protein kinases are required for the general control of carbon and nitrogen uptake and metabolism

Eukaryotic Cell 9: 1881-1890

Hoeberichts FA, Perez-Valle J, Montesinos C, Mulet JM, Planes MD, Hueso G, Yenush L, Sharma SC, Serrano R (2010)

The role of K+ and H+ transport systems during glucose- and H2O2-induced cell death in Saccharomyces cerevisiae

Yeast 27: 713-725

Muñoz-Bertomeu J, Cascales-Miñana B, Mulet JM, Baroja-Fernández E, Pozueta-Romero J, Kuhn JM, Segura J, Ros R (2009)

Plastidial Glyceraldehyde-3-Phosphate Dehydrogenase Deficiency Leads to Altered Root Development and Affects the Sugar and Amino Acid Balance in Arabidopsis

Plant Physiology 151: 541-558

Gimeno J, Gadea J, Forment J, Pérez-Valle J, Santiago J, Martínez-Godoy MA, Yenush L, Bellés JM, Brumós J, Colmenero-Flores JM, Talón M, Serrano R (2009)

Shared and novel molecular responses of mandarin to drought

Plant Molecular Biology 70: 403- 420

Alejandro S, Rodriguez PL, Bellés JM, Yenush L, Garcia-Sanchez MJ, Fernandez JA, Serrano R (2007)

An Arabidopsis quiescin-sulfhydryl oxidase regulates cation homeostasis at the root symplast-xylem interface

EMBO Journal 26: 3203-3215

Pérez-Valle J, Jenkins H, Merchan S, Montiel V, Ramos J, Sharma S, Serrano R, Yenush L (2007)

Key role for intracellular K+ and protein kinases Sat4/Hal4 and Hal5 in the plasma membrane stabilization of yeast nutrient transporters

Molecular and Cellular Biology 27: 5725-5736

Portillo F, Mulet JM, Serrano R (2005)

A Role for the non-phosphorylated Form of Yeast Snf1: Tolerance to Toxic Cations and Activation of Potassium Transporter

FEBS letters 579: 512-516

Yenush L, Merchan S, Holmes J, Serrano R (2005)

pH-Responsive, posttranslational regulation of the Trk1 potassium transporter by the type 1-related Ppz1 phosphatase

Molecular and Cellular Biology 25: 8683-8692

Mulet JM, Alemany B, Ros R, Calvete JJ, Serrano R (2004)

Expression of a Plant Serine O-acetyltransferase in Saccharomyces cerevisiae Confers Osmotic Tolerance and Creates and Alternative Pathway for Cysteine Biosynthesis

Yeast 21: 303-312

Merchan S, Bernal D, Serrano R, Yenush L (2004)

Response of the yeast Mpk1 MAP kinase pathway to increases in internal turgor pressure caused by loss of the Ppz protein phosphatases

Eukaryotic Cell 3: 100-107

Mulet JM, Alejandro S, Romero C, Serrano R (2004)

The Trehalose Pathway and Intracellular Glucose Phosphates as Modulators of Potassium Transport and General Cation Homeostasis in Yeast

Yeast 21: 569-582

Ruiz A, Yenush L, Ariño J (2003)

Regulation of ENA1 Na(+)-ATPase Gene Expression by the Ppz1 Protein Phosphatase Is Mediated by the Calcineurin Pathway

Eukaryotic Cell 2: 937-948

Rausell A, Kanhonou R, Yenush L, Serrano R, Ros R (2003)

The translation initiation factor eIF1A is an important determinant in the tolerance to NaCl stress in yeast and plants

Plant Journal 34: 1-11

Patel S, Yenush L, Rodriguez PL, Serrano R, Blundell TL (2002)

Crystal Structure of an Enzyme Displaying both Inositol-polyphosphate-1-Phosphatase and 3´-Phosphoadenosine-5´-phosphate Phosphatase Activities: A Novel Target of Lithium Therapy

Journal of Molecular Biology 315: 677-685

Mulet JM, Serrano R (2002)

Simultaneous Determination of Potassium and Rubidium Content in Yeast

Yeast 19: 1295-1298

Yenush L, Mulet JM, Ariño J, Serrano R (2002)

The Ppz Protein Phosphatases are Key Regulators of K+ and pH Homeostasis: Implications for Salt Tolerance, Cell Wall Integrity and Cell Cycle Progression

EMBO Journal 21: 920-929

Forment J, Mulet JM, Vicente O, Serrano R (2002)

The Yeast SR Protein Kinase Sky1p Modulates Salt Tolerance, Membrane Potential and the Trk1,2 Potassium Transporter

Biochimica et Biophysica Acta 1565: 36-40

Yenush L, Belles JM, Lopez-Coronado JM, Gil-Mascarell R, Serrano R, Rodriguez PL (2000)

A novel target of lithium therapy

FEBS Letters 467: 321-325

Albert A, Martinez-Ripoll M, Espinosa-Ruiz A, Yenush L, Culiañez-Macia FA, Serrano R (2000)

The X-ray structure of AtHal3 provides the structural basis for the activity of a regulatory subunit involved in signal transduction

Structure 8: 961-969

Mulet JM, Leube MP, Kron SJ, Ríos G, Fink GR, Serrano R (1999)

A Novel Mechanism of Ion Homeostasis and Salt Tolerance in Yeast: the Hal4 and Hal5 Protein Kinases Modulate the Trk1- Trk2 Potassium Transporter

Molecular and Cellular Biology 19: 3328-3337