Antagonism between phytohormone signalling underlies the variation in disease susceptibility of tomato plants under elevated CO2

Zhang, Shuai; Li, Xin; Sun, Zaoyi; Shao, Shujun; Hu, Lingfei; Meng, Yahan; Zhou, Yanhong; Xia, Xiaojian; Yu, Jingquan; Shi, Kai

doi:10.1093/jxb/eru538

Cited by 106 publications

(103 citation statements)

References 62 publications

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“…While previous studies reporting high-CO 2 -induced increases in SA have described unchanged or diminished contents of JA (Casteel et al, 2012;Huang et al, 2012;Zhang et al, 2015), we observed that both pathways were up-regulated together in Arabidopsis. The induction of these pathways by increased CO 2 is accompanied by enhanced resistance to both Pto and B. cinerea, the latter observation contrasting with results obtained in tomato, in which high CO 2 was reported to substantially increase sensitivity to the fungus .…”

Section: Discussioncontrasting

confidence: 95%

“…Significant increases in SA contents during growth at high CO 2 have been reported in tobacco, soybean, and tomato (Matros et al, 2006;Casteel et al, 2012;Huang et al, 2012;Zhang et al, 2015). Our results confirm these observations in other crop species and in Arabidopsis.…”

Section: Discussionsupporting

confidence: 90%

“…Specific plant-pathogen interactions may be affected differently by high CO 2 , and any one interaction may be influenced by CO 2 levels in multiple ways. Increased CO 2 could influence plant disease resistance by altering the nutritional value of plant tissues, by modifying pathways involved in plant resistance, or by modulating pathogen vigor and virulence (Hibberd et al, 1996;Lake and Wade, 2009;Melloy et al, 2010Melloy et al, , 2014Helfer, 2014;Zhang et al, 2015). During longterm exposure to increases in CO 2 in an agronomic setting, secondary effects could result from changes in plant development or canopy density (Eastburn et al, 2010(Eastburn et al, , 2011.…”

mentioning

confidence: 99%

“…Despite this, there have been very few detailed studies focused on how high CO 2 modulates plant defense pathways. Growth at high CO 2 increases SA in tomato (Solanum lycopersicum) and soybean (Casteel et al, 2012;Huang et al, 2012;Zhang et al, 2015). Certain secondary metabolites also were increased in tobacco (Nicotiana tabacum) grown at high CO 2 , although only very slight effects on SA were observed (Matros et al, 2006).…”

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confidence: 99%

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High CO2 primes plant biotic stress defences through redox-linked pathways

Mhamdi

Noctor

2016

Plant Physiol.

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Industrial activities have caused tropospheric CO 2 concentrations to increase over the last two centuries, a trend that is predicted to continue for at least the next several decades. Here, we report that growth of plants in a CO 2 -enriched environment activates responses that are central to defense against pathogenic attack. Salicylic acid accumulation was triggered by high-growth CO 2 in Arabidopsis (Arabidopsis thaliana) and other plants such as bean (Phaseolus vulgaris). A detailed analysis in Arabidopsis revealed that elevated CO 2 primes multiple defense pathways, leading to increased resistance to bacterial and fungal challenge. Analysis of gene-specific mutants provided no evidence that activation of plant defense pathways by high CO 2 was caused by stomatal closure. Rather, the activation is partly linked to metabolic effects involving redox signaling. In support of this, genetic modification of redox components (glutathione contents and NADPH-generating enzymes) prevents full priming of the salicylic acid pathway and associated resistance by high CO 2 . The data point to a particularly influential role for the nonphosphorylating glyceraldehyde-3-phosphate dehydrogenase, a cytosolic enzyme whose role in plants remains unclear. Our observations add new information on relationships between high CO 2 and oxidative signaling and provide novel insight into plant stress responses in conditions of increased CO 2 .

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Section: Discussioncontrasting

confidence: 95%

Section: Discussionsupporting

confidence: 90%

mentioning

confidence: 99%

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High CO2 primes plant biotic stress defences through redox-linked pathways

Mhamdi

Noctor

2016

Plant Physiol.

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“…Free-air CO 2 enrichment (FACE) studies have indicated that elevated CO 2 increases plant susceptibility to certain fungal species (Kobayashi et al, 2006; Melloy et al, 2010) but reduces susceptibility to certain bacterial pathogens and some fungal species (Jwa and Walling, 2001; Zhang et al, 2015). These results were largely explained by the cross-talk between jasmonic acid (JA)- and salicylic acid (SA)-signaling pathways, which are vital for plant resistance against different types of pathogens (Eastburn et al, 2011; Zhang et al, 2015). Elevated CO 2 increased plant resistance against Potato virus Y in tobacco and Tomato yellow leaf curl virus (TYLCV) in tomato (Matros et al, 2006; Huang et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

The Contrasting Effects of Elevated CO2 on TYLCV Infection of Tomato Genotypes with and without the Resistance Gene, Mi-1.2

et al. 2016

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Elevated atmospheric CO2 typically enhances photosynthesis of C3 plants and alters primary and secondary metabolites in plant tissue. By modifying the defensive signaling pathways in host plants, elevated CO2 could potentially affect the interactions between plants, viruses, and insects that vector viruses. R gene-mediated resistance in plants represents an efficient and highly specific defense against pathogens and herbivorous insects. The current study determined the effect of elevated CO2 on tomato plants with and without the nematode resistance gene Mi-1.2, which also confers resistance to some sap-sucking insects including whitefly, Bemisia tabaci. Furthermore, the subsequent effects of elevated CO2 on the performance of the vector whiteflies and the severity of Tomato yellow leaf curl virus (TYLCV) were also determined. The results showed that elevated CO2 increased the biomass, plant height, and photosynthetic rate of both the Moneymaker and the Mi-1.2 genotype. Elevated CO2 decreased TYLCV disease incidence and severity for Moneymaker plants but had the opposite effect on Mi-1.2 plants whether the plants were agroinoculated or inoculated via B. tabaci feeding. Elevated CO2 increased the salicylic acid (SA)-dependent signaling pathway on Moneymaker plants but decreased the SA-signaling pathway on Mi-1.2 plants when infected by TYLCV. Elevated CO2 did not significantly affect B. tabaci fitness or the ability of viruliferous B. tabaci to transmit virus regardless of plant genotype. The results indicate that elevated CO2 increases the resistance of Moneymaker plants but decreases the resistance of Mi-1.2 plants against TYLCV, whether the plants are agroinoculated or inoculated by the vector. Our results suggest that plant genotypes containing the R gene Mi-1.2 will be more vulnerable to TYLCV and perhaps to other plant viruses under elevated CO2 conditions.

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