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. 2017 Jul 10;17(1):118.
doi: 10.1186/s12870-017-1069-4.

Jasmonate-mediated defence responses, unlike salicylate-mediated responses, are involved in the recovery of grapevine from bois noir disease

Anna Rita Paolacci  1 , Giulio Catarcione  1 , Luisa Ederli  2 , Claudia Zadra  3 , Stefania Pasqualini  2 , Maurizio Badiani  4 , Rita Musetti  5 , Simonetta Santi  5 , Mario Ciaffi  6
Affiliations

Jasmonate-mediated defence responses, unlike salicylate-mediated responses, are involved in the recovery of grapevine from bois noir disease

Anna Rita Paolacci et al. BMC Plant Biol. .

Erratum in

Abstract

Background: Bois noir is an important disease of grapevine (Vitis vinifera L.), caused by phytoplasmas. An interesting, yet elusive aspect of the bois noir disease is "recovery", i.e., the spontaneous and unpredictable remission of symptoms and damage. Because conventional pest management is ineffective against bois noir, deciphering the molecular bases of recovery is beneficial. The present study aimed to understand whether salicylate- and jasmonate-defence pathways might have a role in the recovery from the bois noir disease of grapevine.

Results: Leaves from healthy, bois noir-diseased and bois noir-recovered plants were compared, both in the presence (late summer) and absence (late spring) of bois noir symptoms on the diseased plants. Analyses of salicylate and jasmonate contents, as well as the expression of genes involved in their biosynthesis, signalling and action, were evaluated. In symptomatic diseased plants (late summer), unlike symptomless plants (late spring), salicylate biosynthesis was increased and salicylate-responsive genes were activated. In contrast, jasmonate biosynthesis and signalling genes were up-regulated both in recovered and diseased plants at all sampling dates. The activation of salicylate signalling in symptomatic plants might have antagonised the jasmonate-mediated defence response by suppressing the expression of jasmonate-responsive genes.

Conclusions: Our results suggest that grapevine reacts to phytoplasma infection through salicylate-mediated signalling, although the resultant full activation of a salicylate-mediated response is apparently ineffective in conferring resistance against bois noir disease. Activation of the salicylate signalling pathway that is associated with the presence of bois noir phytoplasma seems to antagonise the jasmonate defence response, by failing to activate or suppressing both the expression of some jasmonate responsive genes that act downstream of the jasmonate biosynthetic pathway, as well as the first events of the jasmonate signalling pathway. On the other hand, activation of the entire jasmonate signalling pathway in recovered plants suggests the potential importance of jasmonate-regulated defences in preventing bois noir phytoplasma infections and the subsequent development of bois noir disease. Thus, on one hand, recovery could be achieved and maintained over time by preventing the activation of defence genes associated with salicylate signalling, and on the other hand, by activating jasmonate signalling and other defence responses.

Keywords: Bois noir disease and recovery; Grapevine; Jasmonate; Phytoplasmas; Plant-pathogen interactions; Salicylate; Stolbur; Vitis vinifera L.

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Conflict of interest statement

Ethics approval and consent to participate

Samples were collected in a private vineyard, according to an informal agreement between the owner and the Plant Pathology scientists of the Department of Agricultural, Food, Environmental and Animal Sciences of the University of Udine, for monitoring this vineyard for bois noir disease since 2006.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Free and total salicylate (SA) in the leaves of bois noir-diseased (D), healthy (H), and recovered (R) Chardonnay grapevines, collected when symptoms were apparent (August 2011 and 2012) or still latent (June 2012). Each value represents the mean ± SE of five biological replicates (n = 5). Different letters, when present, denote significant differences at P ≤ 0.01 (lowercase or common) or at P ≤ 0.05 (uppercase or capital); regular font or bold letters are used for free or total salicylate, respectively
Fig. 2
Fig. 2
Levels of 12-oxo-phytodienoic acid (OPDA), jasmonate (JA) and methyl-jasmonate (MeJA) in the grapevine leaves of Fig. 1. Statistics as in Fig. 1. Letters denoting significant differences are in regular font or bold font for JA or MeJA, respectively
Fig. 3
Fig. 3
Relative expression levels of genes coding for phenylalanine ammonia-lyase (PAL) and isochorismate synthase (ICS) in the grapevine leaves of Fig. 1. For each gene, relative expression levels were calculated by setting a value of 1, as the lowest value among bois noir-diseased (D), healthy (H), or recovered (R) plants. The expression data of each gene were normalised using the geometric average of the two reference genes VvEF1α and VvGAPDH. Their normalised relative values are presented as the mean ± SD of five biological replicates, each of which was analysed in triplicate (n = 15). Statistics as in Fig. 1
Fig. 4
Fig. 4
Relative expression levels of genes coding for lipoxygenase (LOX), allene oxide synthase (AOS), allene oxide cyclase (AOC), OPDA reductase (OPR) and jasmonate carboxyl methyltransferase (JMT) in the grapevine leaves of Fig. 1. Calibration, normalisation, sample replication and statistics as in Fig. 3
Fig. 5
Fig. 5
Relative expression levels of genes coding for components of the salicylate (SA) or jasmonate (JA) signalling pathways, namely nonexpressor of PR1 (NPR1), enhanced disease susceptibility (EDS1), myelocytomatosis (MYC2) and jasmonate ZIM-domain (JAZ), in the grapevine leaves of Fig. 1. Calibration, normalisation, sample replication and statistics as in Fig. 3
Fig. 6
Fig. 6
Relative expression levels of genes coding for WRKY transcription factors in the grapevine leaves of Fig. 1. Responsiveness to salicylate (SA) or jasmonate (JA), when known, is indicated. Calibration, normalisation, sample replication and statistics as in Fig. 3
Fig. 7
Fig. 7
Relative expression levels of genes coding for pathogenesis-related (PR) proteins in the grapevine leaves of Fig. 1. PR gene families and their responsiveness to salicylate (SA) or jasmonate (JA), when known, are indicated. Calibration, normalisation, sample replication and statistics as in Fig. 3
Fig. 8
Fig. 8
Relative expression levels of genes coding for stilbene synthase (STS) and MYB transcription factors in the grapevine leaves of Fig. 1. The STS phylogenetic groups are indicated. Calibration, normalisation, sample replication and statistics as in Fig. 3
Fig. 9
Fig. 9
Relative expression levels of genes coding for calchone synthase in the grapevine leaves of Fig. 1. Calibration, normalisation, sample replication and statistics as in Fig. 3
Fig. 10
Fig. 10
Simplified model showing the salicylate-jasmonate interplay in the bois noir disease of grapevine. Plants react to phytoplasma infection by salicylate-mediated signalling, failing to activate or antagonising the jasmonate-mediated defence response, which leads to the development of bois noir symptoms and disease (left panel). On the other hand, activation of the entire jasmonate signalling pathway, together with counteraction of salicylate signalling and action, inhibits the development of symptoms and phytoplasma disease, leading to recovery from bois noir (right panel). Acknowledgements: the TEM image showing phytoplasmas infecting a phloem cell is publicly available at: http://dna-barcoding.blogspot.it/2012/12/phytoplasma.html. The picture showing the insect vector Hyalesthes obsoletus is publicly available at: https://www.naturamediterraneo.com/forum/topic.asp?TOPIC_ID=119017
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