Host Genotype and Colonist Arrival Order Jointly Govern Plant Microbiome Composition and Function

Area of Science:

• Ecology
• Microbiology
• Plant Pathology

Background:

• Host-associated microbiomes significantly influence host health and fitness.
• Microbiome assembly is influenced by historical contingency, particularly species arrival order (priority effects), which can overshadow host-driven deterministic processes.
• The impact of priority effects on host health and the role of host intraspecific variation in modulating these effects remain unclear.

Purpose of the Study:

• To investigate whether species arrival order affects microbiome composition and subsequent host disease susceptibility.
• To determine if host genotype influences the trajectory of microbiome assembly under priority effects.
• To explore if microbiome assembly history can impact host disease susceptibility independently of current microbiome composition.

Main Methods:

• A greenhouse inoculation experiment using the black cottonwood (Populus trichocarpa) foliar microbiome.
• Manipulation of host genotype and the colonization order of common foliar fungi.
• Quantification of microbiome assembly using fungal marker gene sequencing and measurement of host susceptibility to Melampsora × columbiana leaf rust.

Main Results:

• The influence of species arrival order on microbiome composition and disease susceptibility was dependent on the host genotype.
• Microbiome assembly history affected host disease susceptibility, even when microbiome composition at pathogen exposure was similar.
• The interactive effects of species arrival order and host genotype can decouple microbiome community composition from its ecological function (disease resistance).

Conclusions:

• Priority effects in microbiome assembly are consequential for host health, and their impact is modulated by host genotype.
• Host genotype plays a critical role in determining how historical microbial colonization events shape plant disease susceptibility.
• These findings underscore the importance of stochastic processes in microbiome assembly and identify host factors that influence susceptibility to these effects.