Drought Stress Interacts With Powdery Mildew Infection in Tomato

Under field conditions, plants are often exposed to more than one stress factor at the same time, and therefore need to adapt to different combinations of stresses. Crosstalk between responses to abiotic and biotic stresses is known to occur, and the interaction between stress responses can be positive or negative. We studied the interaction of drought stress and powdery mildew (PM) infection in tomatoes using near-isogenic tomato lines (NILs) carrying the Ol-1, ol-2, or Ol-4 gene that confers resistance to tomato PM caused by Oidium neolycopersici. Our study demonstrated that drought-induced growth reduction was not further reduced by powdery mildew infection. Drought stress, however, decreased fungal infection in the susceptible genotype Moneymaker (MM) with fungal biomass tending to decrease further as the drought severity increased. Drought stress did not affect PM resistance levels of resistant NIL carrying ol-2 (a mutant of the tomato susceptibility Mlo gene) and Ol-4 an NLR (nucleotide-binding site-LRR) R gene associated with a fast hypersensitivity response (HR) but tended to slightly decrease disease levels of NIL-Ol-1 (no gene characterized yet, associated with a slow HR following PM infection). At the molecular level, genes involved in abscisic acid (ABA), salicylic acid (SA), and ethylene pathways were highly induced under combined stress indicating the involvement of ABA, SA, and ethylene in the crosstalk between abiotic and biotic stress. Messenger RNA expression of the ABA-responsive dehydrin SlTAS14 was induced under drought and combined stress with the highest induction under combined stress, and resistant NIL lines showed higher expression levels than MM. The expression of SlNCED (involved in ABA synthesis) was also upregulated under drought and highly induced under combined stress. Expression levels of pathogen responsive gene SlPR1 (an indicator of the SA pathway) and SlACS (involved in ethylene synthesis) were highly induced under powdery mildew infection in MM and the Ol-1 and were induced the most under combined stress in these lines. Taken together, these findings indicate that drought stress can interact with and influence PM infection in tomatoes in a resistance type-dependent manner. The role of hormonal signaling pathways in the crosstalk between drought stress and PM infection is further discussed.

[1]  Kalyani M Barbadikar,et al.  Improvement of Upland Rice Variety by Pyramiding Drought Tolerance QTL with Two Major Blast Resistance Genes for Sustainable Rice Production , 2021 .

[2]  R. Togawa,et al.  Defining the combined stress response in wild Arachis , 2021, Scientific Reports.

[3]  S. He,et al.  Crops of the future: building a climate-resilient plant immune system. , 2021, Current opinion in plant biology.

[4]  Tim Iven,et al.  ABA-Dependent Salt Stress Tolerance Attenuates Botrytis Immunity in Arabidopsis , 2020, Frontiers in Plant Science.

[5]  Marco Zarattini,et al.  Every cloud has a silver lining: how abiotic stresses affect gene expression in plant-pathogen interactions , 2020, Journal of experimental botany.

[6]  D. Martínez,et al.  Physiological and Proteomic Changes in the Apoplast Accompany Leaf Senescence in Arabidopsis , 2020, Frontiers in Plant Science.

[7]  M. Senthil-Kumar,et al.  Impact of drought stress on simultaneously occurring pathogen infection in field-grown chickpea , 2019, Scientific Reports.

[8]  Trevor M. Nolan,et al.  AP2/ERF Transcription Factor Regulatory Networks in Hormone and Abiotic Stress Responses in Arabidopsis , 2019, Front. Plant Sci..

[9]  R. Garrido-Oter,et al.  Balancing trade-offs between biotic and abiotic stress responses through leaf age-dependent variation in stress hormone cross-talk , 2019, Proceedings of the National Academy of Sciences.

[10]  R. Visser,et al.  The Role of Tomato WRKY Genes in Plant Responses to Combined Abiotic and Biotic Stresses , 2018, Front. Plant Sci..

[11]  Sudipta Ray,et al.  Dehydrins Impart Protection against Oxidative Stress in Transgenic Tobacco Plants , 2018, Front. Plant Sci..

[12]  R. Visser,et al.  Plant behaviour under combined stress: tomato responses to combined salinity and pathogen stress. , 2018, The Plant journal : for cell and molecular biology.

[13]  R. M. Rivero,et al.  Reactive oxygen species, abiotic stress and stress combination. , 2017, The Plant journal : for cell and molecular biology.

[14]  R. Panstruga,et al.  mlo-Based Resistance: An Apparently Universal "Weapon" to Defeat Powdery Mildew Disease. , 2017, Molecular plant-microbe interactions : MPMI.

[15]  R. Visser,et al.  Ethylene and Abscisic Acid Signaling Pathways Differentially Influence Tomato Resistance to Combined Powdery Mildew and Salt Stress , 2017, Front. Plant Sci..

[16]  Jean-Benoit Morel,et al.  Transcriptional Basis of Drought-Induced Susceptibility to the Rice Blast Fungus Magnaporthe oryzae , 2016, Front. Plant Sci..

[17]  R. Visser,et al.  Responses to combined abiotic and biotic stress in tomato are governed by stress intensity and resistance mechanism , 2016, Journal of experimental botany.

[18]  F. Ortego,et al.  Drought-Stressed Tomato Plants Trigger Bottom–Up Effects on the Invasive Tetranychus evansi , 2016, PloS one.

[19]  M. Tucker,et al.  Examination of the Abscission-Associated Transcriptomes for Soybean, Tomato, and Arabidopsis Highlights the Conserved Biosynthesis of an Extensible Extracellular Matrix and Boundary Layer , 2015, Front. Plant Sci..

[20]  M. Senthil-Kumar,et al.  The interactive effects of simultaneous biotic and abiotic stresses on plants: mechanistic understanding from drought and pathogen combination. , 2015, Journal of plant physiology.

[21]  W. Weckwerth,et al.  Ectopic overexpression of the cell wall invertase gene CIN1 leads to dehydration avoidance in tomato , 2014, Journal of experimental botany.

[22]  R. Proels,et al.  Cell-wall invertases, key enzymes in the modulation of plant metabolism during defence responses. , 2014, Molecular plant pathology.

[23]  Richard G. F. Visser,et al.  Enhancing crop resilience to combined abiotic and biotic stress through the dissection of physiological and molecular crosstalk , 2014, Front. Plant Sci..

[24]  R. Visser,et al.  Powdery Mildew Resistance in Tomato by Impairment of SlPMR4 and SlDMR1 , 2013, PloS one.

[25]  K. Mysore,et al.  Drought Stress Acclimation Imparts Tolerance to Sclerotinia sclerotiorum and Pseudomonas syringae in Nicotiana benthamiana , 2013, International journal of molecular sciences.

[26]  D. Cipollini,et al.  Overlapping defense responses to water limitation and pathogen attack and their consequences for resistance to powdery mildew disease in garlic mustard, Alliaria petiolata , 2011, Chemoecology.

[27]  Sophia Sonnewald,et al.  Cell Wall-Bound Invertase Limits Sucrose Export and Is Involved in Symptom Development and Inhibition of Photosynthesis during Compatible Interaction between Tomato and Xanthomonas campestris pv vesicatoria[W][OA] , 2008, Plant Physiology.

[28]  K. Shinozaki,et al.  Antagonistic Interaction between Systemic Acquired Resistance and the Abscisic Acid–Mediated Abiotic Stress Response in Arabidopsis[W] , 2008, The Plant Cell Online.

[29]  B. Asselbergh,et al.  Global switches and fine-tuning-ABA modulates plant pathogen defense. , 2008, Molecular plant-microbe interactions : MPMI.

[30]  S. Somerville,et al.  Senescence-associated genes induced during compatible viral interactions with grapevine and Arabidopsis. , 2007, Journal of experimental botany.

[31]  M. Höfte,et al.  Influence of drought, salt stress and abscisic acid on the resistance of tomato to Botrytis cinerea and Oidium neolycopersici , 2006 .

[32]  E. Weis,et al.  Photosynthesis and carbohydrate metabolism in tobacco leaves during an incompatible interaction with Phytophthora nicotianae , 2005 .

[33]  Yuling Bai,et al.  Tomato defense to Oidium neolycopersici: dominant Ol genes confer isolate-dependent resistance via a different mechanism than recessive ol-2. , 2005, Molecular plant-microbe interactions : MPMI.

[34]  H. Meziane,et al.  The salicylic acid‐dependent defence pathway is effective against different pathogens in tomato and tobacco , 2004 .

[35]  Yuling Bai,et al.  QTLs for tomato powdery mildew resistance (Oidium lycopersici) in Lycopersicon parviflorum G1.1601 co-localize with two qualitative powdery mildew resistance genes. , 2003, Molecular plant-microbe interactions : MPMI.

[36]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[37]  A. Newton,et al.  Temporary partial breakdown of mlo‐resistance in spring barley by sudden relief of soil water‐stress under field conditions: the effects of genetic background and mlo allele , 1998 .

[38]  A. Newton,et al.  Temporary partial breakdown of Mlo‐resistance in spring barley by the sudden relief of soil water stress , 1996 .

[39]  Y. Saijo,et al.  Plant immunity in signal integration between biotic and abiotic stress responses. , 2019, The New phytologist.

[40]  C. Geilfus.  Drought Stress , 2019, Controlled Environment Horticulture.

[41]  Guo-Yan Zhang,et al.  The WRKY transcription factor WRKY8 promotes resistance to pathogen infection and mediates drought and salt stress tolerance in Solanum lycopersicum. , 2019, Physiologia plantarum.

[42]  F. Ortego,et al.  Drought stress in tomato increases the performance of adapted and non-adapted strains of Tetranychus urticae. , 2017, Journal of insect physiology.

[43]  R. Visser,et al.  Naturally occurring broad-spectrum powdery mildew resistance in a Central American tomato accession is caused by loss of mlo function. , 2008, Molecular plant-microbe interactions : MPMI.

[44]  E. Pahlich,et al.  A rapid DNA isolation procedure for small quantities of fresh leaf tissue , 1980 .