Plant developmental stage drives the differentiation in ecological role of the maize microbiome

Chao Xiong, Brajesh K. Singh, Ji‑Zheng He, Yan‑Lai Han, Pei‑Pei Li, Li‑Hua Wan, Guo‑Zhong Meng, Si‑Yi Liu, Jun‑Tao Wang, Chuan‑Fa Wu, An‑Hui Ge, Li-Mei Zhang

Research output: Contribution to journalArticlepeer-review

220 Citations (Scopus)

Abstract

Background: Plants live with diverse microbial communities which profoundly affect multiple facets of host performance, but if and how host development impacts the assembly, functions and microbial interactions of crop microbiomes are poorly understood. Here we examined both bacterial and fungal communities across soils, epiphytic and endophytic niches of leaf and root, and plastic leaf of fake plant (representing environment-originating microbes) at three developmental stages of maize at two contrasting sites, and further explored the potential function of phylloplane microbiomes based on metagenomics. Results: Our results suggested that plant developmental stage had a much stronger influence on the microbial diversity, composition and interkingdom networks in plant compartments than in soils, with the strongest effect in the phylloplane. Phylloplane microbiomes were co-shaped by both plant growth and seasonal environmental factors, with the air (represented by fake plants) as its important source. Further, we found that bacterial communities in plant compartments were more strongly driven by deterministic processes at the early stage but a similar pattern was for fungal communities at the late stage. Moreover, bacterial taxa played a more important role in microbial interkingdom network and crop yield prediction at the early stage, while fungal taxa did so at the late stage. Metagenomic analyses further indicated that phylloplane microbiomes possessed higher functional diversity at the early stage than the late stage, with functional genes related to nutrient provision enriched at the early stage and N assimilation and C degradation enriched at the late stage. Coincidently, more abundant beneficial bacterial taxa like Actinobacteria, Burkholderiaceae and Rhizobiaceae in plant microbiomes were observed at the early stage, but more saprophytic fungi at the late stage. Conclusions: Our results suggest that host developmental stage profoundly influences plant microbiome assembly and functions, and the bacterial and fungal microbiomes take a differentiated ecological role at different stages of plant development. This study provides empirical evidence for host exerting strong effect on plant microbiomes by deterministic selection during plant growth and development. These findings have implications for the development of future tools to manipulate microbiome for sustainable increase in primary productivity.
Original languageEnglish
Article number171
Number of pages15
JournalMicrobiome
Volume9
Issue number1
DOIs
Publication statusPublished - 2021

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© The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativeco mmons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

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