Microbe-Associated Molecular Patterns-Triggered Root Responses Mediate Beneficial Rhizobacterial Recruitment in Arabidopsis

Venkatachalam Lakshmanan,Sherry L Kitto,Harsh P Bais,Yi-Huang Hsueh,Yu-Sung Wu,Daniel B Kearns,Jeffrey L Caplan

doi:10.1104/pp.112.200386

Abstract

This study demonstrated that foliar infection by Pseudomonas syringae pv tomato DC3000 induced malic acid (MA) transporter (ALUMINUM-ACTIVATED MALATE TRANSPORTER1 [ALMT1]) expression leading to increased MA titers in the rhizosphere of Arabidopsis (Arabidopsis thaliana). MA secretion in the rhizosphere increased beneficial rhizobacteria Bacillus subtilis FB17 (hereafter FB17) titers causing an induced systemic resistance response in plants against P. syringae pv tomato DC3000. Having shown that a live pathogen could induce an intraplant signal from shoot-to-root to recruit FB17 belowground, we hypothesized that pathogen-derived microbe-associated molecular patterns (MAMPs) may relay a similar response specific to FB17 recruitment. The involvement of MAMPs in triggering plant innate immune response is well studied in the plant's response against foliar pathogens. In contrast, MAMPs-elicited plant responses on the roots and the belowground microbial community are not well understood. It is known that pathogen-derived MAMPs suppress the root immune responses, which may facilitate pathogenicity. Plants subjected to known MAMPs such as a flagellar peptide, flagellin22 (flg22), and a pathogen-derived phytotoxin, coronatine (COR), induced a shoot-to-root signal regulating ALMT1 for recruitment of FB17. Micrografts using either a COR-insensitive mutant (coi1) or a flagellin-insensitive mutant (fls2) as the scion and ALMT1(pro):β-glucuronidase as the rootstock revealed that both COR and flg22 are required for a graft transmissible signal to recruit FB17 belowground. The data suggest that MAMPs-induced signaling to regulate ALMT1 is salicylic acid and JASMONIC ACID RESISTANT1 (JAR1)/JASMONATE INSENSITIVE1 (JIN1)/MYC2 independent. Interestingly, a cell culture filtrate of FB17 suppressed flg22-induced MAMPs-activated root defense responses, which are similar to suppression of COR-mediated MAMPs-activated root defense, revealing a diffusible bacterial component that may regulate plant immune responses. Further analysis showed that the biofilm formation in B. subtilis negates suppression of MAMPs-activated defense responses in roots. Moreover, B. subtilis suppression of MAMPs-activated root defense does require JAR1/JIN1/MYC2. The ability of FB17 to block the MAMPs-elicited signaling pathways related to antibiosis reflects a strategy adapted by FB17 for efficient root colonization. These experiments demonstrate a remarkable strategy adapted by beneficial rhizobacteria to suppress a host defense response, which may facilitate rhizobacterial colonization and host-mutualistic association.

Highlights

Plant roots are the first organs that come in contact with diverse belowground microflora.Rhizospheric microbes, which utilize plant root exudates for growth and multiplication (Lugtenberg et al., 2001; Bais et al, 2006; Rudrappa et al, 2008a), are attracted to the rhizosphere, and may have either beneficial or deleterious effects on the plant
To determine if a foliar spray of microbe-associated molecular patterns (MAMPs) could influence the recruitment of beneficial rhizosphere bacteria, root-specific colonization was measured in the presence and absence of different
Twenty-day-old Arabidopsis wild type Col-0 (WT) and ALMT1 knock out plants were rhizo-inoculated with the beneficial rhizobacteria, FB17, and subsequently foliar sprayed with different MAMPs and phytotoxin COR

Summary

Introduction

Plant roots are the first organs that come in contact with diverse belowground microflora.Rhizospheric microbes, which utilize plant root exudates for growth and multiplication (Lugtenberg et al., 2001; Bais et al, 2006; Rudrappa et al, 2008a), are attracted to the rhizosphere, and may have either beneficial or deleterious effects on the plant. Several other types of beneficial soil-borne microbes, such as plant growth-promoting rhizobacteria (PGPR) and fungi, can stimulate plant growth by suppressing plant diseases (van Loon et al, 1998) or insect herbivory (van Oosten et al, 2008). The biological control activity is exerted either directly through antagonism of soil-borne pathogens or indirectly by eliciting a plant-mediated resistance response (van Loon et al, 1998; Pozo and Azcón- Aguilar, 2007). SAR is controlled by the salicylic acid (SA)-dependent signaling pathway, and its onset involves local and systemic increases in endogenously synthesized SA, leading to activation of the regulatory protein NPR1 and the subsequent NPR1-dependent expression of genes encoding pathogenesis-related (PR) proteins, including PR1, PR2, and PR5 (van Loon and van Strien, 1999). Non-pathogenic PGPRs regulate ISR by jasmonic acid (JA)- and ethylene (ET)-dependent signaling pathways and are associated with the downstream regulation of plant defensin 1.2 (PDF1.2)

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