Plant-to-plant communication triggered by systemin primes anti-herbivore resistance in tomato

Mariangela Coppola, Pasquale Cascone, Valentina Madonna, Ilaria Di Lelio, Francesco Esposito, Concetta Avitabile, Alessandra Romanelli, Emilio Guerrieri, Alessia Vitiello, Francesco Pennacchio, Rosa Rao, Giandomenico Corrado
2017 Scientific Reports  
Plants actively respond to herbivory by inducing various defense mechanisms in both damaged (locally) and non-damaged tissues (systemically). In addition, it is currently widely accepted that plantto-plant communication allows specific neighbors to be warned of likely incoming stress (defense priming). Systemin is a plant peptide hormone promoting the systemic response to herbivory in tomato. This 18-aa peptide is also able to induce the release of bioactive Volatile Organic Compounds, thus
more » ... promoting the interaction between the tomato and the third trophic level (e.g. predators and parasitoids of insect pests). In this work, using a combination of gene expression (RNA-Seq and qRT-PCR), behavioral and chemical approaches, we demonstrate that systemin triggers metabolic changes of the plant that are capable of inducing a primed state in neighboring unchallenged plants. At the molecular level, the primed state is mainly associated with an elevated transcription of pattern -recognition receptors, signaling enzymes and transcription factors. Compared to naïve plants, systemin-primed plants were significantly more resistant to herbivorous pests, more attractive to parasitoids and showed an increased response to wounding. Small peptides are nowadays considered fundamental signaling molecules in many plant processes and this work extends the range of downstream effects of this class of molecules to intraspecific plant-to-plant communication. Plants have developed multiple defense strategies in a continuous co-evolution with pests. Plant defense mechanisms can be expressed constitutively or induced upon injury 1 . On the basis of the mode of action, defense traits are also distinguished in direct and indirect 1,2 . The former includes, for instance, physical barriers and metabolites that directly interfere with pests, while the latter involves any plant trait that attracts natural enemies of pests, such as predators and parasitoids 1,2 . Systemin is an 18 amino acid (aa) hormone that was firstly identified as a limited range mobile inducer in the wound response in tomato 3 . This peptide is released from a 200 aa precursor, called prosystemin, which is encoded by a single-copy inducible gene 4 . The overexpression of prosystemin cDNA in tomato generates a systemic signal that activates defense genes 5 . It has been proposed that systemin and jasmonic acid (JA) interact through an amplification loop to propagate a long-distance wound signal 6,7 . Although systemin was isolated by exploiting its ability to strongly induce protease inhibitors (PIs) 6 , further studies indicated that this peptide stimulates a wider transcriptome reprogramming, affecting the expression of genes involved in different hormone-regulated pathways 8 . The constitutive accumulation of prosystemin increases the resistance of plants not only against lepidopteran larvae but also against some fungi and aphids 5, 8, 9 . Moreover, prosystemin overexpressing plants are more attractive to natural enemies of pests 10,11 because of the release of various bioactive Volatile Organic Compounds (VOCs) 10 , known to be typically used by predators and parasitoids of phytophagous insects to locate their prey 12 . The constitutive increase of indirect defenses in absence of pests could be of little use from an applied point of view, because the attraction of natural enemies not associated with the presence of potential hosts results in dispersion of natural enemies due to lack of motivation 13 . Therefore, it is also interesting to assess whether the Published: xx xx xxxx OPEN www.nature.com/scientificreports/ 2 ScIentIFIc REPoRTS | 7: 15522 | induction of systemin-can prime the adjacent plants and make them able to mount a more effective defense reaction. Manipulating plant response to biotic stressors by tuning the systemin molecular network may open the way to novel sustainable strategies for plant protection. Priming is a physiological process through which the functions and activities of an unstressed plant are dedicated to support a more rapid and robust response to a probable future challenge 14,15 . Priming may be trigged by different cues such as pathogens, insect pests, molecules of microbial origin, synthetic substances and abiotic stress 16 . Molecular mechanisms linked to priming are diverse and involve chromatin modification for faster activation of defense genes and epigenetic memory 17 . Activation of proteins involved in signal transduction, receptor accumulation and increased levels of some defense compounds also represent common events in priming 17,18 . Priming should not be limited to the expression of defense-related genes, as it may involve other plant responses 14 . Many studies on priming anti-herbivory defense have primarily focused on Herbivore Induced Plant Volatile (HIPVs), since they are also associated to intra-plant, co-specific and interspecific communication 15 . However, information on plant-endogenous signals that can trigger plant-to-plant communication is in comparison more limited. Moreover, differences between priming signal pathways and direct induced defences as well as their mechanistic similarities have not been fully elucidated. Since systemin regulates direct and indirect defenses in tomato 5,10 , the aim of this work was to study if systemin can trigger plant-to-plant communication. Specifically, we wanted to address whether systemin overexpression or exogenous application is able to prime a defense response in unchallenged neighboring plants, and whether this alerted state improves resistance against herbivorous pests and plant response to wounding. Moreover, we aimed to provide insights into the molecular aspects that characterize the primed state in tomato.
doi:10.1038/s41598-017-15481-8 pmid:29138416 pmcid:PMC5686165 fatcat:ad45epi6afcvbeykbb4wb57k7u