Abstract

Most field-grown plants are surrounded by microbes, especially from the soil. Some of these, including bacteria, fungi and nematodes, specifically manipulate the growth and development of their plant hosts, primarily for the formation of structures housing the microbes in roots. These developmental processes require the correct localization of the phytohormone auxin, which is involved in the control of cell division, cell enlargement, organ development and defense, and is thus a likely target for microbes that infect and invade plants. Some microbes have the ability to directly synthesize auxin. Others produce specific signals that indirectly alter the accumulation of auxin in the plant by altering auxin transport. This review highlights root–microbe interactions in which auxin transport is known to be targeted by symbionts and parasites to manipulate the development of their host root system. We include case studies for parasitic root–nematode interactions, mycorrhizal symbioses as well as nitrogen fixing symbioses in actinorhizal and legume hosts. The mechanisms to achieve auxin transport control that have been studied in model organisms include the induction of plant flavonoids that indirectly alter auxin transport and the direct targeting of auxin transporters by nematode effectors. In most cases, detailed mechanisms of auxin transport control remain unknown.

Highlights

  • The rhizosphere is colonized by a multitude of microbial species, many of which interact with plants.the soil microbiome, which defines the specific microbial populations having close associations with a plant root system, has been termed the plant’s second genome [1], and is likely to expand the ability of the root system to respond to its environment

  • This complex initiates the removal of the AUXIN RESISTANT/INDOLE-3-ACETIC ACID (AUX/indole-3-acetic acid (IAA)) family of repressors from the cis elements of auxin responsive genes, and subsequent ubiquitination and degradation, activating auxin-induced responses in the cell [11,12]

  • Another mechanism for auxin relocation into a developing feeding structure includes increased auxin import through the AUX/LAX family of auxin import proteins, similar to auxin transport into cortical cells positioned in front of lateral root primordia through LAX3 during lateral root emergence [43,134] (Table 1)

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Summary

Introduction

The rhizosphere is colonized by a multitude of microbial species, many of which interact with plants. The binding of auxin to the TIR1/AFB receptor recruits the SKP, CULLIN, F-BOX-CONTAINING COMPLEX (SCF) that interacts with the former to produce the ubiquitin-ligase (E3) SCFTIR1/AFB complex [11] This complex initiates the removal of the AUXIN RESISTANT/INDOLE-3-ACETIC ACID (AUX/IAA) family of repressors from the cis elements of auxin responsive genes, and subsequent ubiquitination and degradation, activating auxin-induced responses in the cell [11,12]. There are multiple lines of evidence showing auxin manipulation by microorganisms, including but not limited to nodulation, mycorrhization and nematode infection that form the focus of this review [21,22,23,24] In these cases, auxin accumulation is often associated with the rapid proliferation of host cells during post-embryonic root organ formation. The sections focus on our knowledge of auxin transport control in the plant, followed by evidence for the manipulation of these known auxin transport control points by micro-organisms, based on studies from selected well-studied model systems

Auxin Transport Carriers Regulate Plant Development
PIN Proteins
Dynamic Repositioning of PIN Proteins during Developmental Responses
PILS Proteins
Flavonoids are Natural Auxin Transport Modulators
10. Auxin Changes during Mycorrhizal Interactions
10.1. Ectomycorrhizal Symbioses
10.2. Endomycorrhizal Symbioses
11.1. Actinorhizal Symbioses
11.2. Legume-Rhizobium Symbioses
11.3. Involvement of Auxin Transport Carriers during Legume Nodulation
12. Auxin Acts as a Shoot-Root Regulator of Nodule Numbers
Findings
13. Future Questions
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