Inheritance of seed and rhizosphere microbial communities through plant–soil feedback and soil memory

Abstract

Summary Since the discovery of the role of microbes in the phytobiome, microbial communities (microbiota) have been identified and characterized based on host species, development, distribution, and condition. The microbiota in the plant rhizosphere is believed to have been established prior to seed germination and innate immune development. However, the microbiota in seeds has received little attention. Although our knowledge of the distribution of microbiota in plant seeds and rhizosphere is currently limited, the impact of these microbiota is likely to be greater than expected. This minireview suggests a new function of microbial inheritance from the seed to root and from the first generation of plants to the next. Surprisingly, recruitment and accumulation of microbiota by biotic and abiotic stresses affect plant immunity in the next generation through plant–soil feedback and soil memory. To illustrate this process, we propose a new term called ‘microbiota‐induced soil inheritance (MISI).’ A comprehensive understanding of MISI will provide novel insights into plant–microbe interactions and plant immunity inheritance.

Experimental Evidence of Microbial Inheritance in Plants and Transmission Routes from Seed to Phyllosphere and Root

“…Such initial seed-borne differences among the below-and aboveground plant tissues may cause strong priority effects during later development. Our demonstration of partial transmission of the seed microbiome to the roots con rms previous work suggesting that plant seeds are a repository for rhizosphere microbial communities [64], and the high resemblance of the embryonic and phyllosphere microbiome indicates that seeds may play an even larger role as a repository for the phyllosphere microbial community.…”

“…We also hypothesized that the majority of seed-associated microbes would be transient and that only a small fraction of the microbial taxa would be transmitted to the developing seedling [13,26]. We lacked a strong prior on the subsequent distribution of the transmitted microbiome, but some studies have suggested that the composition of seed-associated microorganisms re ects the microbial community in the roots [4,28], while seed transmission to the phyllosphere is more limited [29,30].…”

WITHDRAWN: Genotype-Dependent Recruitment of the Strawberry Holobiome

“…To date, many important questions regarding these associations remain unanswered, especially concerning the factors determining the community assemblage and diversity of the plant microbiome 3 . Increasing evidence suggests that plants can actively recruit a bene cial micro ora to facilitate their adaptation to environmental conditions and changes 3,6,7 . However, further studies are needed to generalize this hypothesis, and enable practical applications, especially for horticultural perennial crops grown in cultural conditions 8 .…”

Microbiota in the Rhizosphere and Seed of Rice From China, With Reference to Their Transmission and Biogeography

“…Although the underlying mechanisms are unclear, the rhizosphere microbiota has shown a resemblance to the seed-associated microbiota in the compositional structure (Nelson et al, 2018). Moreover, recent evidence has confirmed microbial migration between the seed and the rhizosphere, and the two compartments may serve as the microbial repositories for each other (Kong et al, 2019). A comparison between the seed and the rhizosphere microbiota of rice, therefore, would infer the fractional contribution of the two transmission routes to the assembly of indigenous microbiota of rice seeds, and potentially their association with rice development and health.…”