Soil nutrient levels determine the variation of bacterial communities in the rhizosphere of rice under different conditions of climate and genotype

Highlights

• The interaction effects of soil type, climate, and genotype on the rhizosphere microbiome in rice paddies were evaluated.

• Soil nutrient levels determined the variation of bacterial communities in the rhizosphere of rice.

• High OM reduced the dispersion of bacterial communities probably due to loosen the relationships of abundant taxa.

Abstract

The rhizosphere microbiome, which plays a pivotal role in plant productivity, is shaped by both plant-related and environmental factors. However, few studies have evaluated the effects of plant genotype, soil type, climatic factors, and their interactions on the rhizosphere microbiome of rice (Oryza sativa L.). Here we used Illumina sequencing to investigate the bacterial community in the rhizosphere of two rice genotypes grown in three soil types (Albic, Black, and Chernozem) across three climatic regions in northeastern China. Results showed that soil type, followed by climate, was the primary factor in shaping the bacterial community structure, and their interactions significantly influenced α-diversity. Principal component analysis also revealed that the dispersion of bacterial community in albic soil was much lower than that in black and chernozem soils. Additionally, soil nutrients explained approximately 45% of the variation in bacterial communities, suggesting the effects of climate or genotype on the variation of bacterial communities are associated with soil nutrients. Network analysis revealed that the co-occurrence relationships in albic soil were loosened compared with black and chernozem soils. In three soils, the abundant taxa were more located in central positions within the network than the moderate or rare taxa. Moreover, the closeness centrality of abundant taxa displayed a significantly negative with organic matter, implying a more convergence communities in albic soil probably due to the loose co-occurrence relationship of abundant taxa by high organic matter. Our study revealed the underlying mechanism for the stability of bacterial communities in rice rhizosphere with rich organic matter, and provided a basis for improving the soil quality and maintaining the sustainable development of rice production via fertilization.

Introduction

The rhizosphere is a thin soil zone attached to the plant roots where complex plant-microbe interactions take place (Fan et al., 2017). Root-microbe interactions play a critical role in plant growth, health, and adaptability (Zhang et al., 2017). The rhizosphere microbiome can be engineered and managed to be plant-friendly (Ryan et al., 2009; Zhang et al., 2015; Dessaux et al., 2016) and thus act beneficially on agricultural production, such as improving crop nutrient absorption efficiency, contributing to plant tolerance of abiotic stresses, and enhancing plant resistance to pathogen infections (Breidenbach et al., 2016; Bakker et al., 2018; de Vries et al., 2020). To achieve such purposes, better understandings of how environmental factors affect the assembly of the rhizosphere microbiome is highly essential.Rice is one of the major staple crops and provides important dietary sources of protein and carbohydrates for nearly half the world's population (Moe et al., 2019). Understanding the assembly of the rhizosphere microbiome of rice is critical for both sustainable rice production and global food security.

The rhizosphere microbiome is known to be shaped by both environmental and plant-related factors, such as plant genotype, soil type, and climatic factors (Marques et al., 2014; Qiao et al., 2017; de Vries et al., 2018). Remarkable progress has been made in studying the effect of rice genotype on rhizosphere microbiome assembly. For example, Edwards et al. (2015) revealed that selective assembly of the rhizosphere microbial community was strongly affected by rice genotype under controlled greenhouse conditions. Zhang et al. (2019) found that different rice genotypes selected various microorganisms from the bulk soil to shape a unique microbial community in the rhizosphere, and rice plants were able to coordinate the microbial community to obtain nitrogen from the soil for growth. However, few studies have evaluated the effects of soil type and climatic factors on the rhizosphere microbiome of rice (Conrad et al., 2008; Li et al., 2016; Santos-Medellin et al., 2017; Xu et al., 2020), especially how their interactions with the rice genotype may affect the microbiome assembly.

Many studies have investigated the effects of plant genotype and soil type on the rhizosphere microbiomes of crops such as soybean, potato, cotton, and sorghum (Xu et al., 2009; İnceoğlu et al., 2012; Qiao et al., 2017; Schlemper et al., 2017).These studies suggest that some crops have strong selectivity for rhizosphere microbiome assembly, while soil type is the main factor in shaping rhizosphere microbial communities. Crops often selectively recruit beneficial microbes rather than against them (Yan et al., 2017), implying climate as influencing factors on crop growth (Lesk et al., 2016; Asadi et al., 2018; Fahad et al., 2019) may alter the selective preferences of crop for rhizosphere microbiomes. Actually, multiple studies have confirmed that climatic factors such as drought, temperature, and precipitation are recognized as major drivers of shifts in the rhizosphere microbial communities of crops such as wheat, maize, and cotton (Changey et al., 2018; Walters et al., 2018; Ullah et al., 2019). However, few studies have simultaneously investigated the contributions of soil type, climate, and genotype in shaping rhizosphere bacterial community of crops. Furthermore, rice is distinct from the above-mentioned crops as it is typically cultivated in flooded paddy fields, characterized by an oxygenated rhizosphere and anoxic bulk soil, that select for specific microbial groups (Brune, 2000). Therefore, improving our understanding of the effects of rice genotype, soil type, climatic factors, and their interactions on the rhizosphere microbiome assembly in rice paddies seems to be of fundamental importance.

In the present study, we investigated the bacterial community structure in the rhizosphere of rice under different treatments consisting of combinations of two rice genotypes, three soil types, and three climatic regions. We addressed the following questions: 1) Which factor primarily drives the variation of bacterial communities in the rhizosphere of rice? 2) How do their interactions affect the assembly of bacterial communities in the rhizosphere of rice?