Abstract
Plants have evolved the ability to regrow after mechanical defoliation and environmental stresses. However, it is unclear whether and how defoliated plants exploit beneficial microbiota from the soil to promote aboveground regrowth. Here, we compared the defoliation-triggered changes in the root exudation and bacterial microbiome of two rice cultivars (Oryza sativa L ssp.), indica/xian cultivar Minghui63 and japonica/geng cultivar Nipponbare. The results show that reciprocal growth promotion existed between defoliated Minghui63 seedlings and soil bacteria. After the leaves were removed, the Minghui63 seedlings displayed approximately 1.5- and 2.1-fold higher root exudation and leaf regrowth rates, respectively, than did the Nipponbare seedlings. In field trials, Minghui63 and Nipponbare enriched taxonomically and functionally distinct bacteria in the rhizosphere and root. In particular, Minghui63 rhizosphere and root communities depleted bacteria whose functions are related to xenobiotics biodegradation and metabolism. The microbiome data implied that the bacterial family Rhodocyclaceae was specifically enriched during the regrowth of defoliated Minghui63 rice. We further isolated a Rhodocyclaceae strain, Uliginosibacterium gangwonense MDD1, from rice root. Compared with germ-free conditions, MDD1 inoculation promoted the aboveground regrowth of defoliated Minghui63 by 61% but had a weaker effect on Nipponbare plants, suggesting cultivar-specific associations between regrowth-promoting bacteria and rice. This study provides novel insight into microbiota‒root‒shoot communication, which is implicated in the belowground microbiome and aboveground regrowth in defoliated rice. These data will be helpful for microbiome engineering to increase rice resilience to defoliation and environmental stresses.IMPORTANCEAs sessile organisms, plants face a multitude of abiotic and biotic stresses which often result in defoliation. To survive, plants have evolved the ability to regrow leaves after stresses and wounding. Previous studies revealed that the rhizosphere microbiome affected plant growth and stress resilience; however, how belowground microbiota modulates the aboveground shoot regrowth is unclear. To address this question, we used rice, an important crop worldwide, to analyze the role of rhizosphere microbiota in leaf regrowth after defoliation. Our data indicate mutual growth promotion between defoliated rice and rhizosphere bacteria and such beneficial effect is cultivar specific. The microbiome analysis also led us to find a Uliginosibacterium gangwonense strain that promoted rice cv. MH63 leaf regrowth. Our findings therefore present a novel insight into plant-microbiome function and provide beneficial strains that potentially enhance rice stress resilience.