Changes in tolerance and resistance of a plant to insect herbivores under variable water availability

Lin, Po An; Paudel, Sulav; Afzal, Amin; Shedd, Nancy L.; Felton, Gary W.

doi:10.1016/j.envexpbot.2020.104334

Cited by 26 publications

(24 citation statements)

References 45 publications

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“…The ROS signals work downstream from Ca 2+ ( Farooq et al, 2019 ) and the Ca 2+ cyt increase was associated with the upregulation of chloroplastic polyphenol oxidase F ( Solyc08g074630 ) and a peroxidase ( Solyc03g025380 ). Polyphenol oxidase upregulation is involved in tomato resistance to herbivory ( Lin et al, 2021 ) and pathogens ( Zhang and Sun, 2021 ), whereas peroxidase activity was associated to tomato resistance to early blight disease ( Alizadeh-Moghaddam et al, 2020 ). On the opposite, ubiquinol oxidase ( Solyc08g075550 ) and catalase ( Solyc01g100630 ) were downregulated in response to eDNA treatment.…”

Section: Discussionmentioning

confidence: 99%

Extracellular Fragmented Self-DNA Is Involved in Plant Responses to Biotic Stress

2021

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A growing body of evidence indicates that extracellular fragmented self-DNA (eDNA), by acting as a signaling molecule, triggers inhibitory effects on conspecific plants and functions as a damage-associated molecular pattern (DAMP). To evaluate early and late events in DAMP-dependent responses to eDNA, we extracted, fragmented, and applied the tomato (Solanum lycopersicum) eDNA to tomato leaves. Non-sonicated, intact self-DNA (intact DNA) was used as control. Early event analyses included the evaluation of plasma transmembrane potentials (Vm), cytosolic calcium variations (Ca2+cyt), the activity and subcellular localization of both voltage-gated and ligand-gated rectified K+ channels, and the reactive oxygen species (ROS) subcellular localization and quantification. Late events included RNA-Seq transcriptomic analysis and qPCR validation of gene expression of tomato leaves exposed to tomato eDNA. Application of eDNA induced a concentration-dependent Vm depolarization which was correlated to an increase in (Ca2+)cyt; this event was associated to the opening of K+ channels, with particular action on ligand-gated rectified K+ channels. Both eDNA-dependent (Ca2+)cyt and K+ increases were correlated to ROS production. In contrast, application of intact DNA produced no effects. The plant response to eDNA was the modulation of the expression of genes involved in plant–biotic interactions including pathogenesis-related proteins (PRPs), calcium-dependent protein kinases (CPK1), heat shock transcription factors (Hsf), heat shock proteins (Hsp), receptor-like kinases (RLKs), and ethylene-responsive factors (ERFs). Several genes involved in calcium signaling, ROS scavenging and ion homeostasis were also modulated by application of eDNA. Shared elements among the transcriptional response to eDNA and to biotic stress indicate that eDNA might be a common DAMP that triggers plant responses to pathogens and herbivores, particularly to those that intensive plant cell disruption or cell death. Our results suggest the intriguing hypothesis that some of the plant reactions to pathogens and herbivores might be due to DNA degradation, especially when associated to the plant cell disruption. Fragmented DNA would then become an important and powerful elicitor able to trigger early and late responses to biotic stress.

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Section: Discussionmentioning

confidence: 99%

Extracellular Fragmented Self-DNA Is Involved in Plant Responses to Biotic Stress

2021

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“…For our purposes, we used two proxies: fruit yield (i.e., total number of tomatoes produced) and single fruit weight. Both of these metrics are common proxies for tolerance (count: Weinig et al, 2003 ; Martin et al, 2015 ; Lin et al, 2021 ; weight: Welter and Steggall, 1993 ; Olejniczak, 2011 ). Though frequently used, fruit count and weight are just two of many plant traits that shape fitness.…”

Section: Methodsmentioning

confidence: 99%

Characterizing rhizosphere microbial communities associated with tolerance to aboveground herbivory in wild and domesticated tomatoes

2022

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Root-associated microbial communities are well known for their ability to prime and augment plant defenses that reduce herbivore survival or alter behavior (i.e., resistance). In contrast, the role root microbes play in plant tolerance to herbivory, an evolutionarily sustainable alternative to resistance, is overlooked. In this study, we aimed to expand our limited understanding of what role rhizosphere microbial communities play in supporting tolerance to insect damage. Using domesticated tomatoes and their wild ancestors (Solanum spp.), we first documented how tobacco hornworm (Manduca sexta) herbivory impacted tomato fruit production in order to quantify plant tolerance. We then characterized the bacterial and fungal rhizosphere communities harbored by high and low tolerance plants. Wild tomatoes excelled at tolerating hornworm herbivory, experiencing no significant yield loss despite 50% leaf area removal. Their domesticated counterparts, on the other hand, suffered 26% yield losses under hornworm herbivory, indicating low tolerance. Ontogeny (i.e., mid- vs. late-season sampling) explained the most variation in rhizosphere community structure, with tomato line, tolerance, and domestication status also shaping rhizosphere communities. Fungal and bacterial community traits that associated with the high tolerance line include (1) high species richness, (2) relatively stable community composition under herbivory, and (3) the relative abundance of taxa belonging to Stenotrophomonas, Sphingobacterium, and Sphingomonas. Characterizing tolerance-associating microbiomes may open new avenues through which plant defenses are amended in pest management, such as plant breeding efforts that enhance crop recruitment of beneficial microbiomes.

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Section: Bottom-up Approachesmentioning

confidence: 99%

“…Lin, Paudel, Afzal, Shedd, and Felton (2021) studied how lower water availability increased the levels of two tomato plant defensive proteins, trypsin PI and PPO. It was shown how these resistance factors directly influence the consumption of plant tissues and the performance of Manduca sexta (Linnaeus) (Lepidoptera: Sphingidae) a specialist caterpillar (Lin et al, 2021). Furthermore, in conditions of water deficit, the increase in the concentration of glycoalkaloids in the tomato leaves negatively affects survival, pupal weight and larval development time of T. absoluta (Han et al, 2016).…”

Section: Alterations In the Plant Defensive Profile And Their Multitr...mentioning

confidence: 99%

“…The quantity and quality of the plant watering can enhance the plant defence mechanisms thus affecting the plant resistance to herbivores (Dong et al, 2018; Dong et al, 2020; Gutbrodt, Mody, & Dorn, 2011). Lin, Paudel, Afzal, Shedd, and Felton (2021) studied how lower water availability increased the levels of two tomato plant defensive proteins, trypsin PI and PPO. It was shown how these resistance factors directly influence the consumption of plant tissues and the performance of Manduca sexta (Linnaeus) (Lepidoptera: Sphingidae) a specialist caterpillar (Lin et al, 2021).…”

Section: Alterations In the Plant Defensive Profile And Their Multitr...mentioning

confidence: 99%

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Plant defences for enhanced integrated pest management in tomato

Tortorici

Biondi

Pérez‐Hedo

et al. 2022

Annals of Applied Biology

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Plants developed a series of defence mechanisms to counteract the attack of herbivores. These can impact on food‐webs at various trophic levels, in both natural and managed ecosystems, such as crops. The biochemical and ecological bases behind these processes are reviewed here by highlighting the differences in direct and indirect, constitutive and induced defences. In integrated pest management (IPM), several pest control tools are applied in an economically sound way in order to increase the crop resilience and reduce reliance on synthetic pesticides. Plant resistance is thus a crucial aspect of preventive pest control strategies in several agroecosystems, including tomato. In this context, we review the current literature dealing with the physiology and biochemistry of tomato plants in terms of metabolite pathways and multitrophic interactions. We also describe recent advances in plant defence‐based control tools obtained by studying the multitrophic interactions between pests and plants in the tomato system.

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Changes in tolerance and resistance of a plant to insect herbivores under variable water availability

Cited by 26 publications

References 45 publications

Extracellular Fragmented Self-DNA Is Involved in Plant Responses to Biotic Stress

Extracellular Fragmented Self-DNA Is Involved in Plant Responses to Biotic Stress

Characterizing rhizosphere microbial communities associated with tolerance to aboveground herbivory in wild and domesticated tomatoes

Plant defences for enhanced integrated pest management in tomato

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