Interplay between Arabidopsis thaliana Genotype, Plant Growth and Rhizosphere Colonization by Phytobeneficial Phenazine-Producing Pseudomonas chlororaphis

Abstract

Rhizosphere colonization by phytobeneficial Pseudomonas spp. is pivotal in triggering their positive effects on plant health. Many Pseudomonas spp. Determinants, involved in rhizosphere colonization, have already been deciphered. However, few studies have explored the role played by specific plant genes in rhizosphere colonization by these bacteria. Using isogenic Arabidopsis thaliana mutants, we studied the effect of 20 distinct plant genes on rhizosphere colonization by two phenazine-producing P. chlororaphis strains of biocontrol interest, differing in their colonization abilities: DTR133, a strong rhizosphere colonizer and ToZa7, which displays lower rhizocompetence. The investigated plant mutations were related to root exudation, immunity, and root system architecture. Mutations in smb and shv3, both involved in root architecture, were shown to positively affect rhizosphere colonization by ToZa7, but not DTR133. While these strains were not promoting plant growth in wild-type plants, increased plant biomass was measured in inoculated plants lacking fez, wrky70, cbp60g, pft1 and rlp30, genes mostly involved in plant immunity. These results point to an interplay between plant genotype, plant growth and rhizosphere colonization by phytobeneficial Pseudomonas spp. Some of the studied genes could become targets for plant breeding programs to improve plant-beneficial Pseudomonas rhizocompetence and biocontrol efficiency in the field.

Keywords: Arabidopsis; PGPR; Pseudomonas; SALK; colonization; immunity; phenazine; rhizocompetence; rhizosphere; root architecture.

Figure 1

Rhizosphere colonization three weeks following bacterial inoculation with P. chlororaphis subsp. piscium strains ToZa7 and DTR133 for 21 A. thaliana genotypes. Asterisks refer to significant differences between groups. (A,B): nonparametric multiple test procedure for many-to-one comparisons [81], allowing the comparison of all mutants against the wild type. (C): Wilcoxon–Mann–Whitney tests. * p-value < 0.05; ** p-value < 0.01; *** p-value < 0.001; n.s.: non-significant. Bars indicate standard errors (n = 10).

Figure 2

Dry mass of plant aboveground parts three weeks following inoculation with P. chlororaphis subsp. piscium strains ToZa7 and DTR133 for 21 A. thaliana genotypes. Asterisks refer to significant differences between groups defined by Fisher’s least significant difference test. * p-value < 0.05; ** p-value < 0.01; *** p-value < 0.001. Bars indicate standard errors (n = 10). (A) Comparisons between treatments for each plant genotype (graphs have been divided for easy layout). (B) Uninoculated plant mutants compared to the wild type.

Figure 3

Dry mass of roots and aboveground parts of 21 A. thaliana genotypes grown in sterile sand (not inoculated). Asterisks refer to significant differences between the wild type and another genotype, defined by Fisher’s least significant difference test. * p-value < 0.05. Bars indicate standard errors (n = 3). (A) Root dry mass of plants grown in sand (uninoculated). (B) Aboveground dry mass of plants grown in sand (uninoculated).

Figure 4

Root system (top) and root hair zone (bottom) of representative uninoculated A. thaliana wild type (left) and shv3 mutant plants (right) grown in sterile sand.