Soil Microbiome of the Guayule (Parthenium Argentatum) Root Zone in Diverse Semi-Arid Agricultural Fields

Abstract

Guayule (P. argentatum) is an arid-adapted, low water-use crop that is currently being proposed as a replacement for traditional high water-use crops, such as cotton and alfalfa in the southwestern United States (US). Guayule is a prime candidate as an alternative crop in the semi-arid southwest as it requires minimal water and nutrient inputs. Guayule is one of approximately 2000 plants that synthesize rubber, and is one of only two plants to be exploited as a commercial source. Guayule has long been considered as an alternative source of rubber, however extensive work is still required to domesticate and establish guayule as a new or alternative crop in the southwestern US. As an alternative crop, guayule will be grown in a variety of fields with potentially different soil properties and environmental conditions, thus understanding the variability of the soil microbiome is important for guayule growth and production. Previous reports have demonstrated that guayule is highly susceptible to fungal and oomycete soilborne pathogens, with soil moisture and soil texture playing a large role in disease incidence and severity. Species of Fusarium, Macrophomina, Phymatotrichum, Rhizoctonia, Sclerotinia, Sclerotium, and Verticillium have been identified as putative soilborne fungal pathogens of guayule; however, very little information exists on the overall distribution of fungal pathogens in guayule agricultural fields. The purpose of this dissertation was to participate in a two-year irrigation field trial that was part of a large interdisciplinary US Department of Agriculture research effort entitled Sustainable Bioeconomy for Arid Regions. This field trial was conducted at two distinct agricultural fields in southern Arizona with identical experimental designs and similar environmental conditions, but different soil textures to examine: 1) the prevalence and distribution of fungal soilborne pathogens, and 2) the overall soil microbiome. Samples were collected from the guayule root zone in the spring of 2018, and 2019. The internal transcribed spacer (ITS) amplicon sequencing successfully detected four putative guayule fungal soilborne pathogens at both field locations: Fusarium solani, Fusarium oxysporum, Macrophomina phaseolina, and Rhizoctonia solani. The distribution of fungal pathogens across both fields was highly variable, with no significant associations between irrigation treatment and fungal pathogen relative abundance. However, potential disease symptoms were observed on plants in one D150 plot, the highest drip irrigation rate, at the MAC field. F. solani relative abundance in the root zone of symptomatic plants was high; up to 53%, relative to other pathogen relative abundances, suggesting an association with this pathogen and guayule mortality under high irrigation levels in sandy soils where saturated conditions occur. Unlike M. phaseolina, and Rhizoctonia spp, the presence and relative abundance of F. solani did not decrease with plant establishment in either the MAC or Eloy fields. Thus, successful guayule establishment suppresses the relative abundance of some but not all putative fungal pathogens. The data also suggest a significant impact of soil texture on the distribution of the F. oxysporum phylotype. The bacterial/archaeal soil community was analyzed at both field locations to provide a temporal analysis during guayule establishment. Little is known regarding the soil microbiome of guayule and its effect/s on guayule productivity; however, it is well established that microbes enhance plant growth by facilitating nutrient acquisition, suppressing soilborne diseases, and conferring abiotic stress tolerance. The soil microbiome was significantly different at the course phylogenetic level when comparing the two field locations (p < 0.001). The soil microbiome was also significantly different when comparing the two sampling years within each location (p < 0.001). No significant differences in richness and diversity were observed, with the exception of MAC year 1 samples vs. MAC year 2 samples (p = 0.04). Major differences in the relative abundance of phyla between field locations indicates a strong influence of soil texture on the soil microbiome, and major phylum differences between sampling years indicates guayule establishment does not have a similar effect on the soil microbiome in both fields. Of particular interest was the ammonia-oxidizing archaea Thaumarchaeota, whose relative abundance in both fields was not typical for arid, alkaline soils. This research has demonstrated that two significantly different microbial communities support guayule growth in these two different fields. Taken together, these studies provide the first description and novel insights into guayule root zone soil microbial communities that are potentially relevant to guayule growth and productivity.