Rhizosphere Bacterial Networks, but Not Diversity, Are Impacted by Pea-Wheat Intercropping.

Barbara Pivato,Thibault Guégan,Christophe Lecomte,Nathalie Moutier,Samuel Jacquiod,Amélie Semblat,Judith Burstin,Philippe Lemanceau,Florence Deau,Juliette Martin

doi:10.3389/fmicb.2021.674556

Abstract

Plant-plant associations, notably cereal-legume intercropping, have been proposed in agroecology to better value resources and thus reduce the use of chemical inputs in agriculture. Wheat-pea intercropping allows to decreasing the use of nitrogen fertilization through ecological processes such as niche complementarity and facilitation. Rhizosphere microbial communities may account for these processes, since they play a major role in biogeochemical cycles and impact plant nutrition. Still, knowledge on the effect of intecropping on the rhizosphere microbiota remains scarce. Especially, it is an open question whether rhizosphere microbial communities in cereal-legume intercropping are the sum or not of the microbiota of each plant species cultivated in sole cropping. In the present study, we assessed the impact of wheat and pea in IC on the diversity and structure of their respective rhizosphere microbiota. For this purpose, several cultivars of wheat and pea were cultivated in sole and intercropping. Roots of wheat and pea were collected separately in intercropping for microbiota analyses to allow deciphering the effect of IC on the bacterial community of each plant species/cultivar tested. Our data confirmed the well-known specificity of the rhizosphere effect and further stress the differentiation of bacterial communities between pea genotypes (Hr and hr). As regards the intercropping effect, diversity and structure of the rhizosphere microbiota were comparable to sole cropping. However, a specific co-occurrence pattern in each crop rhizosphere due to intercropping was revealed through network analysis. Bacterial co-occurrence network of wheat rhizosphere in IC was dominated by OTUs belonging to Alphaproteobacteria, Bacteroidetes and Gammaproteobacteria. We also evidenced a common network found in both rhizosphere under IC, indicating the interaction between the plant species; this common network was dominated by Acidobacteria, Alphaproteobacteria, and Bacteroidetes, with three OTUs belonging to Acidobacteria, Betaproteobacteria and Chloroflexi that were identified as keystone taxa. These findings indicate more complex rhizosphere bacterial networks in intercropping. Possible implications of these conclusions are discussed in relation with the functioning of rhizosphere microbiota in intercropping accounting for its beneficial effects.

Highlights

Rhizosphere is a dynamic zone of interactions between microorganisms and their host plants (Hiltner, 1903; Hartmann et al, 2008)
Microbial α-diversity was significantly higher in wheat than in pea rhizosphere in the first experiment including seven wheat cultivars (Wilcoxon-Mann-Whitney, p = 7.46e-04; p = 3.3e-04; p = 1.27e-03 for Observed, Shannon and Simpson diversity indices, respectively), but not in the second only including two wheat cultivars (Supplementary Figure 3A)
Differences between the species in the pooled data sets were explained by five Operational taxonomic Units (OTUs) of Proteobacteria, three Alphaproteobacteria and two Betaproteobacteria (Burkholderiales order) that were preferentially associated with pea (Supplementary Data Sheet 1)

Summary

Introduction

Rhizosphere is a dynamic zone of interactions between microorganisms and their host plants (Hiltner, 1903; Hartmann et al, 2008). Rhizosphere ecology has received a great deal of attention with major progress made in understanding plant-microorganism interactions (Philippot et al, 2013; Guttman et al, 2014). They have allowed to demonstrate the specificity of the socalled rhizosphere effect at the species (Lemanceau et al, 1995; Grayston et al, 1998; Berg and Smalla, 2009; Lakshmanan et al, 2014; Tkacz et al, 2020) and even at the genotype level, for maize (Peiffer et al, 2013), soybean (Zhong et al, 2019), and medic (Pivato et al, 2007). Identification of plant and microbial traits involved in positive feedback loops has become a major target for plantbreeding in order to take better advantage of beneficial effects of rhizosphere microbiota (Wei and Jousset, 2017) for decreasing the use of chemical inputs in a more sustainable agriculture (Lemanceau et al, 2015)

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Results

Conclusion