Tomato SR/CAMTA transcription factors SlSR1 and SlSR3L negatively regulate disease resistance response and SlSR1L positively modulates drought stress tolerance

Abstract

BackgroundThe SR/CAMTA proteins represent a small family of transcription activators that play important roles in plant responses to biotic and abiotic stresses. Seven SlSR/CAMTA genes were identified in tomato as tomato counterparts of SR/CAMTA; however, the involvement of SlSRs/CAMTAs in biotic and abiotic stress responses is not clear. In this study, we performed functional analysis of the SlSR/CAMTA family for their possible functions in defense response against pathogens and tolerance to drought stress.ResultsExpression of SlSRs was induced with distinct patterns by Botrytis cinerea and Pseudomonas syringae pv. tomato (Pst) DC3000. Virus-induced gene silencing (VIGS)-based knockdown of either SlSR1 or SlSR3L in tomato resulted in enhanced resistance to B. cinerea and Pst DC3000 and led to constitutive accumulation of H2O2, elevated expression of defense genes, marker genes for pathogen-associated molecular pattern-triggered immunity, and regulatory genes involved in the salicylic acid- and ethylene-mediated signaling pathways. Furthermore, the expression of SlSR1L and SlSR2L in detached leaves and whole plants was significantly induced by drought stress. Silencing of SlSR1L led to decreased drought stress tolerance, accelerated water loss in leaves, reduced root biomass and attenuated expression of drought stress responsive genes in tomato. The SlSR1 and SlSR3L proteins were localized in the nucleus of plant cells when transiently expressed in Nicotiana benthamiana and had transcriptional activation activity in yeast.ConclusionsVIGS-based functional analyses demonstrate that both SlSR1 and SlSR3L in the tomato SlSR/CAMTA family are negative regulators of defense response against B. cinerea and Pst DC3000 while SlSR1L is a positive regulator of drought stress tolerance in tomato.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-014-0286-3) contains supplementary material, which is available to authorized users.

Calmodulin-binding transcription activators and perspectives for applications in biotechnology

“…Furthermore, the expression of SlSR1L and SlSR2L in tomato seedlings is significantly upregulated by drought stress. However, exogenous ABA does not affect the expression of SlSR1L (Li et al 2014). Thus, it is likely that an unknown mechanism existed in CAMTA-mediated drought stress response in tomato.…”

“…oryzae and the rice blast fungus Magnaporthe grisea (Koo et al 2009). In tomato, CAMTA transcription factors, SlSR1 and SlSR3L, also negatively regulate pathogen resistance responses (Li et al 2014). In summary, CAMTA genes may be good resistance candidates for crop breeding.…”

Tomato SlERF.A1, SlERF.B4, SlERF.C3 and SlERF.A3, Members of B3 Group of ERF Family, Are Required for Resistance to Botrytis cinerea

“…Spores were collected from 10-day-old plates by rinsing the culture with 1% maltose buffer, filtered through bi-layered cheesecloth and adjusted to 2 × 10 5 spores/ml for inoculation (Li et al, 2014a). For gene expression analyses, 4-week-old plants were inoculated by foliar spraying with spore suspension or with same volume of 1% maltose buffer as a mock-inoculation control and leaf samples were collected at different time points after inoculation.…”

“…It was shown that ABA regulates the immunity to B. cinerea in tomato through modulating the cuticle permeability and pectin composition in cell wall or suppressing the SA-mediated signaling pathway or the production of nitric oxide (Audenaert et al, 2002; Asselbergh et al, 2007; Curvers et al, 2010; Sivakumaran et al, 2016). A number of genes encoding receptor-like protein kinase TPK1b, transcriptional factors SHINE3, AIM1, SlDRW1, SlSRN1, SlSR1, and SlSR3L (Abuqamar et al, 2008, 2009; Buxdorf et al, 2014; Li et al, 2014a; Liu et al, 2014a,b), histone H2B monoubiquitination enzymes SlHUB1 and SlHUB2 (Zhang Y. et al, 2015), mitogen-activated protein kinase kinase SlMKK2 and SlMKK4 (Li et al, 2014b), phosphatidylinositol-phospholipase SlPLC2 (Gonorazky et al, 2016), NADPH oxidase SlRbohB (Li X. et al, 2015), 12-oxophytodienoate reductase SlOPR3 (Scalschi et al, 2015) and matrix metalloproteinase Sl3-MMP (Li D. et al, 2015) have been identified to play important roles in tomato immunity against B. cinerea . Enzymes involved in biosynthesis of vitamin B6 and trehalose-6-phosphate as well as concurrent over-activation of cytosolic glutamine synthetase and γ-aminobutyric acid shunt are also involved in tomato immune response to B. cinerea (Seifi et al, 2013; Zhang et al, 2014, 2016).…”

Identification and Mode of Inheritance of Quantitative Trait Loci for Secondary Metabolite Abundance in Tomato

“…A second possibility is that the divergence of pathways is considerably greater in S. pennellii, and this may lead to a rerouting of carbon into alternate metabolites thereby reducing the pool sizes of the core pathway intermediates. Given that transcriptional control of secondary metabolism has been demonstrated to be quite complex, at least occasionally (for instance, see Li et al, 2014), a third possibility is that primary metabolism is simply under more constrained evolutionary pressures, while secondary metabolism might be under more diversifying selection. While we favor the former two hypotheses, we cannot currently formally exclude any of them.…”