Precipitation increases the abundance of fungal plant pathogens in Eucalyptus phyllosphere

Abstract

Understanding the current and future distributions of plant pathogens is critical to predict the plant performance and related economic benefits in the changing environment. Yet, little is known about the roles of environmental drivers in shaping the profiles of fungal plant pathogens in phyllosphere, an important habitat of microbiomes on Earth. Here, using a largescale investigation of Eucalyptus phyllospheric microbiomes in Australia and the multiple linear regression model, we show that precipitation is the most important predictor of fungal taxonomic diversity and abundance. The abundance of fungal plant pathogens in phyllosphere exhibited a positive linear relationship with precipitation. With this empirical dataset, we constructed current and future atlases of phyllosphere plant pathogens to estimate their spatial distributions under different climate change scenarios. Our atlases indicate that the abundance of fungal plant pathogens would increase especially in the coastal regions with up to 100-fold increase compared with the current abundance. These findings advance our understanding of the distributions of fungal plant pathogens in phyllospheric microbiomes under the climate change, which can improve our ability to predict and mitigate their impacts on plant productivity and economic losses.

Contrasting ecological processes shape the Eucalyptus phyllosphere bacterial and fungal community assemblies

“…For example, some beneficial phyllosphere microorganisms can promote plant growth by providing nutrients and cofactors (e.g., non‐protein compounds that act as catalysts of enzyme's activity), enhancing plant hormone production, and increasing plant tolerance to stresses (e.g., drought) through contributing to the fitness of plants 14,17–19 . On the other hand, pathogenic phyllosphere microorganisms can threaten plant health and cause detrimental impacts on plant growth and performance 20,21 . Phyllosphere microorganisms also play crucial roles in global biogeochemical cycles by contributing to nitrogen fixation and decomposition of organic materials 22 .…”

“…14,[17][18][19] On the other hand, pathogenic phyllosphere microorganisms can threaten plant health and cause detrimental impacts on plant growth and performance. 20,21 Phyllosphere microorganisms also play crucial roles in global biogeochemical cycles by contributing to nitrogen fixation and decomposition of organic materials. 22 The knowledge gap about how phyllosphere microbial community assemblies are shaped by different ecological processes greatly impedes our ability to understand the ecological functions of phyllosphere microbiota and to utilize phyllosphere microbial communities for controlling plant disease and increasing crop production.…”

Organic fertilization regimes suppress fungal plant pathogens through modulating the resident bacterial and protistan communities

“…Potential fungal plant pathogens were predicted with the FUNGuild database, 38 which has been widely used in a number of recent studies. 4,5,9 Potential fungal plant pathogens were identified using a FUNGuild assignment which contained 'pathotroph' and were classified into 'highly probable' or 'probable' categories in this study. 9,38 Raw sequences have been deposited in the NCBI Sequence Read Archive (SRA) under the accession number PRJNA648662 (SRP273724).…”

“…Outbreaks of plant diseases caused by soil-borne fungal and oomycete pathogens are predicted to result in a considerable drop in global crop production. [1][2][3] It is estimated that fungal plant pathogens may further increase their proportions under future climate scenarios (e.g., climate warming and increased precipitation) at global or continental scales, 4,5 with unknown consequences for stable agricultural production and global food security. 6,7 Despite the functional and economical importance of fungal plant pathogens and their ubiquitous presence in soil, however, we have limited knowledge of the key factors modulating their occurrence in the plant-soil systems and the efficient methods to control their environmental occurrence.…”

“…10,11 Plant-soil microbiome interactions span from deleterious (e.g., fungal plant pathogens) to neutral to highly beneficial (e.g., plant beneficial microbes) to the plant, 12 with far-reaching consequences for plant performance, fitness and ecosystem functioning. 5,13 More importantly, plant-associated beneficial microbes are known to be important contributors to enhancing host's resistance against soil-borne plant pathogens, 12,14,15 possibly through competition with pathogens for niches, direct antagonism via production of antibiotics or volatiles, induction of systemic or induced resistance via production of compounds such as salicylic acid, 16 or directly predating pathogenic microbes. [17][18][19] Given the critical role of plant-microorganism and microorganism-microorganism interactions in disease suppression, 17 it is a promising direction to optimize plant-soil-microbe partnerships to enhance soil protection against fungal pathogens.…”