Transcriptomic Responses of Rhizobium phaseoli to Root Exudates Reflect Its Capacity to Colonize Maize and Common Bean in an Intercropping System.

José Luis Aguirre-Noyola,Michel Geovanni Santiago-Martínez,Esperanza Martínez-Romero,Mónica Rosenblueth

doi:10.3389/fmicb.2021.740818

José Luis Aguirre-Noyola, Michel Geovanni Santiago-Martínez + Show 2 more

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https://doi.org/10.3389/fmicb.2021.740818

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Abstract

Corn and common bean have been cultivated together in Mesoamerica for thousands of years in an intercropping system called “milpa,” where the roots are intermingled, favoring the exchange of their microbiota, including symbionts such as rhizobia. In this work, we studied the genomic expression of Rhizobium phaseoli Ch24-10 (by RNA-seq) after a 2-h treatment in the presence of root exudates of maize and bean grown in monoculture and milpa system under hydroponic conditions. In bean exudates, rhizobial genes for nodulation and degradation of aromatic compounds were induced; while in maize, a response of genes for degradation of mucilage and ferulic acid was observed, as well as those for the transport of sugars, dicarboxylic acids and iron. Ch24-10 transcriptomes in milpa resembled those of beans because they both showed high expression of nodulation genes; some genes that were expressed in corn exudates were also induced by the intercropping system, especially those for the degradation of ferulic acid and pectin. Beans grown in milpa system formed nitrogen-fixing nodules similar to monocultured beans; therefore, the presence of maize did not interfere with Rhizobium–bean symbiosis. Genes for the metabolism of sugars and amino acids, flavonoid and phytoalexin tolerance, and a T3SS were expressed in both monocultures and milpa system, which reveals the adaptive capacity of rhizobia to colonize both legumes and cereals. Transcriptional fusions of the putA gene, which participates in proline metabolism, and of a gene encoding a polygalacturonase were used to validate their participation in plant–microbe interactions. We determined the enzymatic activity of carbonic anhydrase whose gene was also overexpressed in response to root exudates.

Highlights

Associated maize (Zea mays) and common bean (Phaseolus vulgaris) crops have been extensively used in agriculture for thousands of years in Mesoamerica
To identify rapid rhizobial responses in a 2-h exudate exposure to bean and maize root exudates from monoculture or milpa system (Figure 1), a whole transcriptome analysis of R. phaseoli Ch24-10 was performed under four conditions: with bean root exudates, maize roots exudates, root exudates from milpa, and N-free Fahraeus solution
Because bacterial populations inhabiting the rhizoplane have different metabolisms depending on the area of the root that they colonize (Kragelund et al, 1997), transcriptomes of bacteria growing in plant exudates offer the advantage of being more homogeneous and reproducible

Summary

Introduction

Associated maize (Zea mays) and common bean (Phaseolus vulgaris) crops have been extensively used in agriculture for thousands of years in Mesoamerica. These associated crops are called “milpa” (from the Nahuatl words: “milli” which means cultivated plot and “pan” which means upon) (RodríguezRobayo et al, 2020). Milpa systems have a high agricultural value for farmers as they provide a large food volume per area and a diet rich in nutrients, vitamins and bioactive compounds (Méndez-Flores et al, 2021; Novotny et al, 2021). A reason for this is that maize has a deeper root system than beans, which allows the milpa to explore a greater volume of soil to absorb nutrients and water (AlbinoGarduño et al, 2015). Maize–bean intercropping is more effective in controlling diseases and insect pests (Fininsa, 1996) and soil fertility is conserved better than in monoculture crops (Alfonso et al, 1997)

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