Alternaria Brassicae Induces Systemic Jasmonate Responses in Arabidopsis Which Travel to Neighboring Plants via a Piriformsopora Indica Hyphal Network and Activate Abscisic Acid Responses.

Khabat Vahabi,Michael Reichelt,Sandra S Scholz,Ralf Oelmüller,Joy M Johnson,Mitsuhiro Matsuo,Alexandra C U Furch,Irena Sherameti,Jonathan Gershenzon

doi:10.3389/fpls.2018.00626

Abstract

Stress information received by a particular local plant tissue is transferred to other tissues and neighboring plants, but how the information travels is not well understood. Application of Alternaria Brassicae spores to Arabidopsis leaves or roots stimulates local accumulation of jasmonic acid (JA), the expression of JA-responsive genes, as well as of NITRATE TRANSPORTER (NRT)2.5 and REDOX RESPONSIVE TRANSCRIPTION FACTOR1 (RRTF1). Infection information is systemically spread over the entire seedling and propagates radially from infected to non-infected leaves, axially from leaves to roots, and vice versa. The local and systemic NRT2.5 responses are reduced in the jar1 mutant, and the RRTF1 response in the rbohD mutant. Information about A. brassicae infection travels slowly to uninfected neighboring plants via a Piriformospora Indica hyphal network, where NRT2.5 and RRTF1 are up-regulated. The systemic A. brassicae-induced JA response in infected plants is converted to an abscisic acid (ABA) response in the neighboring plant where ABA and ABA-responsive genes are induced. We propose that the local threat information induced by A. brassicae infection is spread over the entire plant and transferred to neighboring plants via a P. indica hyphal network. The JA-specific response is converted to a general ABA-mediated stress response in the neighboring plant.

Highlights

Long distance signaling and organ-to-organ communication are essential features of all plants (Huber and Bauerle, 2016)
Since interplant signal transfer requires systemic information flow within a plant, we looked for genes which responded systemically to various threats in preliminary experiments and decided for NRT2.5 and RESPONSIVE TRANSCRIPTION FACTOR1 (RRTF1) as read-out to assay information transfer for radially and axially traveling signals
Since only a low elevation in the NRT2.5 and RRTF1 mRNA levels was observed in the nonconnected distal leaf no. 10, and the response started much later (Dengler, 2006; Kiep et al, 2015), a volatile compound as signal transducer is unlikely (Figure 1A)

Summary

Introduction

Long distance signaling and organ-to-organ communication are essential features of all plants (Huber and Bauerle, 2016). These processes allow information perceived locally to be systemically spread over the entire plant body, and integrated by regulatory networks causing non-cell autonomous responses in neighboring and systemic cells (Suzuki and Mittler, 2012; Fu and Dong, 2013; Kliebenstein, 2014). In Arabidopsis, systemic leaf-to-leaf signaling depends on direct vascular connections of local and systemic leaves, hardwired by the developmental pattern of the rosettes (Dengler, 2006; Mousavi et al, 2013; Salvador-Recatalà et al, 2014; Kiep et al, 2015)

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Conclusion