Jasmonic acid priming of potato uses hypersensitive response-dependent defense and delays necrotrophic phase change against Phytophthora infestans

Highlights

• The treatment with 150 μg mL-1 of jasmonic acid has no adverse effects at the physiological level in potatoes.

• Jasmonic acid signaling modulate changes in stomatal conductance in the plant.

• The jasmonic acid-dependent priming effect works within a specific time window.

• JA priming effect enhances transcription of genes related to HR, ROS and cell wall reinforcement in response to P. infestans.

Abstract

One of the most important diseases affecting potato is late blight, caused by the oomycete Phtytophthora infestans. The use of jasmonic acid has been reported to reduce the progression of the disease in potato, but the defense mechanisms involved in this response are unknown. In this study we described the effect of jasmonic acid as a priming agent over time in the defense response of potato against the invasion of P. infestans. We observed that the initial stimulus generated by the exogenous application of jasmonic acid had an effect on the stomatal conductance of the treated tissue and activated StMYC2 expression. Results reveal a priming effect in plants inoculated 11 days after treatment with jasmonic acid, evidenced by an increased transcriptional induction of defense-associated genes, decrease in the number of necrotic lesions and an evident reduction of lesion area (72.23%). Furthermore, in this study, we show that the tested concentration of jasmonic acid does not have an adverse effect at the physiological level in plants, since variation in stomatal conductance was transient, no change in chlorophyll a fluorescence and no early senescence in leaves was observed.

Introduction

Potato (Solanum tuberosum) is the third most consumed food crop in the world [1]. This species is affected by the pathogen Phytophthora infestans (Mont.) de Bary causing late blight disease, considered the main phytosanitary problem for potato production [2,3]. This disease can generate yield losses of around 40%, even up to 100% in field conditions in susceptible varieties. These losses represent an annual financial loss of approximately € 6 billion [4,5].

Phytophthora infestans (P. infestans) is a hemibiotrophic oomycete with a two-phases infection style. An initial biotrophic infection phase, where the pathogen requires living cells, which is followed by a second necrotrophic phase. In the necrotrophic phase, the pathogen feeds on dead plant tissue. The change of phase occurs at around 24–48 h post infection [6]. The response of the plant against P. infestans causes notable changes at the physiological level, such as reduced photosynthesis, changes in transpiration, changes in membrane permeability, increased respiratory rate, and changes in tissue expression profiles among others [[7], [8], [9], [10]].

The response of plants to biotic stresses is influenced by signaling pathways regulated by plant hormones such as jasmonic acid (JA) and salicylic acid (SA). These hormones coordinate defense induction in plants depending on the type of pathogen [11]. JA activation is generally associated with defense responses against necrotrophic pathogens, as well as with establishment of systemic induced resistance (ISR); on the contrary, biotrophic and hemibiotrophic pathogens responses are dependent on accumulation of SA and are associated with establishment of systemic acquired resistance (SAR) [[12], [13], [14]]. However, evidence accumulate towards the involvement of jasmonic acid in the response to biotrophic pathogens [15,16] and hemibiotrophic pathogens [[17], [18], [19]].

Plant resistance against pathogens may be induced by exposure to an exogenously applied chemical stimulus. The application of chemical compounds acts as a priming stimulus preparing signaling pathways downstream to respond fast and strong, thus improving the defense response of plants against future biotic stresses [[20], [21], [22]]. Various naturally occurring chemical compounds such as: ethylene (ET), salicylic acid (SA), jasmonic acid (JA) and abscisic acid (ABA) and some non-protein amino acids such as: β-aminobutyric acid (BABA) and pipecolic acid have been reported as defense priming agents [23].

Priming and defense responses differ between plant species and the priming stimulus. These compounds enhance the transcriptional activation of defense-associated genes, the accumulation of biologically active signals or molecules (mRNA, amino acids, phenylpropanoids), improvement of the cell wall structure, generation of reactive oxygen species (ROS), among others [21,[24], [25], [26]]. Previous studies have shown that application of JA act as a priming stimulus by improving the defense response in various species, incrementing the expression of defense genes against attacks on hemibiotrophic pathogens [17,18,27,28].

Research towards priming for potato response to biotic and abiotic stress report effects of various molecules [[29], [30], [31]]. However, the short and medium-term side effects have not been thorough fully analyzed. Several of these compounds interact with primary metabolism, and can affect plant growth and development [31,32]. In order to detail the effect of JA in the plant and further describe its role as a priming agent in potato cv. Criolla Colombia against P. infestans, we initially monitored the plant response to JA during 17 days. Then we tested the time required for the plant to achieve priming by inoculating at three different moments during the duration of the experiment, and analyzed the plant responses during challenge with the pathogen at a phenotypical, physiological and transcriptional level. Our results show a priming effect in plants inoculated 11 days after treatment with jasmonic acid, evidenced by a reduction in lesion area, decrease in the number of necrotic lesions and an enhanced transcriptional induction of defense-associated genes.