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1. Specific and conserved patterns of microbiota-structuring by maize benzoxazinoids in the field

   https://doi.org/10.1186/s40168-021-01049-2  

   Cadot, Selma ; Guan, Hang ; Bigalke, Moritz ; Walser, Jean-Claude ; Jander, Georg ; Erb, Matthias ; van der Heijden, Marcel G. ; Schlaeppi, Klaus ( December 2021 , Microbiome)

   null (Ed.)

   Abstract Background Plants influence their root and rhizosphere microbial communities through the secretion of root exudates. However, how specific classes of root exudate compounds impact the assembly of root-associated microbiotas is not well understood, especially not under realistic field conditions. Maize roots secrete benzoxazinoids (BXs), a class of indole-derived defense compounds, and thereby impact the assembly of their microbiota. Here, we investigated the broader impacts of BX exudation on root and rhizosphere microbiotas of adult maize plants grown under natural conditions at different field locations in Europe and the USA. We examined the microbiotas of BX-producing and multiple BX-defective lines in two genetic backgrounds across three soils with different properties. Results Our analysis showed that BX secretion affected the community composition of the rhizosphere and root microbiota, with the most pronounced effects observed for root fungi. The impact of BX exudation was at least as strong as the genetic background, suggesting that BX exudation is a key trait by which maize structures its associated microbiota. BX-producing plants were not consistently enriching microbial lineages across the three field experiments. However, BX exudation consistently depleted Flavobacteriaceae and Comamonadaceae and enriched various potential plant pathogenic fungi in the roots across the different environments. Conclusions These findings reveal that BXs have a selective impact on root and rhizosphere microbiota composition across different conditions. Taken together, this study identifies the BX pathway as an interesting breeding target to manipulate plant-microbiome interactions. 

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2. Polyploidy in creosote bush ( Larrea tridentata ) shapes the biogeography of specialist herbivores

   https://doi.org/10.1111/jbi.13490  

   O'Connor, Timothy K. ; Laport, Robert G. ; Whiteman, Noah K. ( January 2019 , Journal of Biogeography)

   Whole‐genome duplication (polyploidy) can influence the biogeography and ecology of plants that differ in ploidy level (cytotype). Here, we address how two consequences of plant polyploidy (parapatry of cytotypes and altered species interactions) shape the biogeography of herbivorous insects.

   Warm deserts of North America.

   Gall midges (Asphondylia auripilagroup, Diptera: Cecidomyiidae) that attack three parapatric cytotypes of creosote bush (Larrea tridentata, Zygophyllaceae).

   We surveyedAsphondyliaspecies diversity at 177 sites across a 2300‐km extent. After noting a correspondence between the distributions of eightAsphondyliaspecies andL. tridentatacytotypes, we fine‐mappedAsphondyliaspecies range limits with transects spanning cytotype contact zones. We then tested whether plant–insect interactions and/or abiotic factors explain this coincidence by (a) comparing attack rates and gall midge communities on alternative cytotypes in a narrow zone of sympatry and (b) using species distribution models (SDMs) to determine if climatically suitable habitat for each midge species extended beyond cytotype contact zones.

   The range limits of 6/17Asphondyliaspecies (including two novel putative species confirmed withCOIsequencing) perfectly coincided with the contact zone of diploid and tetraploidL. tridentata. One midge species was restricted to diploid host plants while five were restricted to tetraploid and hexaploid host plants. Where diploid and tetraploidL. tridentataare sympatric, cytotype‐restricted midge species more frequently attacked their typical host andAsphondyliacommunity structure differed markedly between cytotypes.SDMs predicted that distributions of cytotype‐restricted midge species were not constrained by climatic conditions near cytotype contact zones.

   Contact zones between plant cytotypes are dispersal barriers for manyAsphondyliaspecies due to plant–insect interactions. The distribution ofL. tridentatacytotypes therefore shapes herbivore species ranges and herbivore community structure across North American deserts. Our results demonstrate that polyploidy in plants can affect the biogeography of ecological communities.

    

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3. Home-field advantage affects the local adaptive interaction between Andropogon gerardii ecotypes and root-associated bacterial communities

   https://doi.org/10.1128/spectrum.00208-23  

   Kazarina, Anna ; Sarkar, Soumyadev ; Thapa, Shiva ; Heeren, Leah ; Kamke, Abgail ; Ward, Kaitlyn ; Hartung, Eli ; Ran, Qinghong ; Galliart, Matthew ; Jumpponen, Ari ; et al ( October 2023 , Microbiology Spectrum)

   Arias, Renee S. (Ed.)

   Due to climate change, drought frequencies and severities are predicted to increase across the United States. Plant responses and adaptation to stresses depend on plant genetic and environmental factors. Understanding the effect of those factors on plant performance is required to predict species’ responses to environmental change. We used reciprocal gardens planted with distinct regional ecotypes of the perennial grassAndropogon gerardiiadapted to dry, mesic, and wet environments to characterize their rhizosphere communities using 16S rRNA metabarcode sequencing. Even though the local microbial pool was the main driver of these rhizosphere communities, the significant plant ecotypic effect highlighted active microbial recruitment in the rhizosphere, driven by ecotype or plant genetic background. Our data also suggest that ecotypes planted at their homesites were more successful in recruiting rhizosphere community members that were unique to the location. The link between the plants’ homesite and the specific local microbes supported the “home field advantage” hypothesis. The unique homesite microbes may represent microbial specialists that are linked to plant stress responses. Furthermore, our data support ecotypic variation in the recruitment of congeneric but distinct bacterial variants, highlighting the nuanced plant ecotype effects on rhizosphere microbiome recruitment. These results improve our understanding of the complex plant host–soil microbe interactions and should facilitate further studies focused on exploring the functional potential of recruited microbes. Our study has the potential to aid in predicting grassland ecosystem responses to climate change and impact restoration management practices to promote grassland sustainability.

   In this study, we used reciprocal gardens located across a steep precipitation gradient to characterize rhizosphere communities of distinct dry, mesic, and wet regional ecotypes of the perennial grassAndropogon gerardii. We used 16S rRNA amplicon sequencing and focused oligotyping analysis and showed that even though location was the main driver of the microbial communities, ecotypes could potentially recruit distinct bacterial populations. We showed that differentA. gerardiiecotypes were more successful in overall community recruitment and recruitment of microbes unique to the “home” environment, when growing at their “home site.” We found evidence for “home-field advantage” interactions between the host and host–root-associated bacterial communities, and the capability of ecotypes to recruit specialized microbes that were potentially linked to plant stress responses. Our study aids in a better understanding of the factors that affect plant adaptation, improve management strategies, and predict grassland function under the changing climate.

    

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4. Host expansion in a specialist herbivore is facilitated by whole‐genome duplication in the host plant

   https://doi.org/10.1111/een.13223  

   Curé, Anne E. ; Althoff, David M. ; Segraves, Kari A. ( December 2022 , Ecological Entomology)

   Host plant shifts are central to diversification in insect herbivores. Many mechanisms can cause host shifts in insects, but one relatively unexplored mechanism is whole‐genome duplication (WGD) in the host plant. WGD, or polyploidy, is common in plants and causes spontaneous changes in physiology, morphology, and palatability that could impact the ability of herbivores to feed and develop on newly formed polyploids (neopolyploids).

   Here the authors tested if WGD affected the preference and performance of the specialist aphid,Acyrthosiphon pisum(pea aphids). Pea aphids seasonally form specialised lineages or ‘host forms’ on many host plant species including alfalfa and red clover. Aphid host forms on alfalfa and red clover naturally exist on different cytotypes of their respective hosts, with red clover aphids feeding on diploid clover and alfalfa aphids feeding on tetraploid alfalfa. Therefore, the authors predicted that these host forms would have a higher preference for and performance on their respective natal host cytotype.

   Neither host form exhibited a preference for a particular cytotype, but there were modest changes in aphid performance based on host cytotype. Specifically, aphids specialised to red clover had higher fecundity on diploid red clover than on neotetraploid red clover. Together, these results showed that both host forms were able to recognise and accept different cytotypes of the two host species, but only one host form experienced trade‐offs in performance when feeding on neotetraploids. These results suggest that WGD may act as a mechanism of host expansion in pea aphids as plants speciate via WGD.

    

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5. Rhizosphere microbial community composition shifts diurnally and in response to natural variation in host clock phenotype

   https://doi.org/10.1128/msystems.01487-21  

   Hubbard, Charley J. ; Harrison, Joshua G. ; McMinn, Robby ; Bennett Ponsford, Julian C. ; Maignien, Lois ; Ewers, Brent ; Weinig, Cynthia ( June 2023 , mSystems)

   Heck, Michelle (Ed.)

   Plant-associated microbial assemblages are known to shift at time scales aligned with plant phenology, as influenced by the changes in plant-derived nutrient concentrations and abiotic conditions observed over a growing season. But these same factors can change dramatically in a sub-24-hour period, and it is poorly understood how such diel cycling may influence plant-associated microbiomes. Plants respond to the change from day to night via mechanisms collectively referred to as the internal “clock,” and clock phenotypes are associated with shifts in rhizosphere exudates and other changes that we hypothesize could affect rhizosphere microbes. The mustardBoechera strictahas wild populations that contain multiple clock phenotypes of either a 21- or a 24-hour cycle. We grew plants of both phenotypes (two genotypes per phenotype) in incubators that simulated natural diel cycling or that maintained constant light and temperature. Under both cycling and constant conditions, the extracted DNA concentration and the composition of rhizosphere microbial assemblages differed between time points, with daytime DNA concentrations often triple what were observed at night and microbial community composition differing by, for instance, up to 17%. While we found that plants of different genotypes were associated with variation in rhizosphere assemblages, we did not see an effect on soil conditioned by a particular host plant circadian phenotype on subsequent generations of plants. Our results suggest that rhizosphere microbiomes are dynamic at sub-24-hour periods, and those dynamics are shaped by diel cycling in host plant phenotype.

   We find that the rhizosphere microbiome shifts in composition and extractable DNA concentration in sub-24-hour periods as influenced by the plant host’s internal clock. These results suggest that host plant clock phenotypes could be an important determinant of variation in rhizosphere microbiomes.

    

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