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Shade, Ashley (Ed.)ABSTRACT We develop a method to artificially select for rhizosphere microbiomes that confer salt tolerance to the model grass Brachypodium distachyon grown under sodium salt stress or aluminum salt stress. In a controlled greenhouse environment, we differentially propagated rhizosphere microbiomes between plants of a nonevolving, highly inbred plant population; therefore, only microbiomes evolved in our experiment, but the plants did not evolve in parallel. To maximize microbiome perpetuation when transplanting microbiomes between plants and, thus, maximize response to microbiome selection, we improved earlier methods by (i) controlling microbiome assembly when inoculating seeds at the beginning of each selection cycle; (ii) fractionating microbiomes before transfer between plants to harvest, perpetuate, and select on only bacterial and viral microbiome components; (iii) ramping of salt stress gradually from minor to extreme salt stress with each selection cycle to minimize the chance of overstressing plants; (iv) using two nonselection control treatments (e.g., nonselection microbial enrichment and null inoculation) that permit comparison to the improving fitness benefits that selected microbiomes impart on plants. Unlike previous methods, our selection protocol generated microbiomes that enhance plant fitness after only 1 to 3 rounds of microbiome selection. After nine rounds of microbiome selection, the effect of microbiomes selected to confer tolerance to aluminum salt stress was nonspecific (these artificially selected microbiomes equally ameliorate sodium and aluminum salt stresses), but the effect of microbiomes selected to confer tolerance to sodium salt stress was specific (these artificially selected microbiomes do not confer tolerance to aluminum salt stress). Plants with artificially selected microbiomes had 55 to 205% greater seed production than plants with unselected control microbiomes. IMPORTANCE We developed an experimental protocol that improves earlier methods of artificial selection on microbiomes and then tested the efficacy of our protocol to breed root-associated bacterial microbiomes that confer salt tolerance to a plant. Salt stress limits growth and seed production of crop plants, and artificially selected microbiomes conferring salt tolerance may ultimately help improve agricultural productivity. Unlike previous experiments of microbiome selection, our selection protocol generated microbiomes that enhance plant productivity after only 1 to 3 rounds of artificial selection on root-associated microbiomes, increasing seed production under extreme salt stress by 55 to 205% after nine rounds of microbiome selection. Although we artificially selected microbiomes under controlled greenhouse conditions that differ from outdoor conditions, increasing seed production by 55 to 205% under extreme salt stress is a remarkable enhancement of plant productivity compared to traditional plant breeding. We describe a series of additional experimental protocols that will advance insights into key parameters that determine efficacy and response to microbiome selection.more » « less
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Abstract Natural populations are characterized by abundant genetic diversity driven by a range of different types of mutation. The tractability of sequencing complete genomes has allowed new insights into the variable composition of genomes, summarized as a species pan‐genome. These analyses demonstrate that many genes are absent from the first reference genomes, whose analysis dominated the initial years of the genomic era. Our field now turns towards understanding the functional consequence of these highly variable genomes. Here, we analysed weighted gene coexpression networks from leaf transcriptome data for drought response in the purple false brome
Brachypodium distachyon and the differential expression of genes putatively involved in adaptation to this stressor. We specifically asked whether genes with variable “occupancy” in the pan‐genome – genes which are either present in all studied genotypes or missing in some genotypes – show different distributions among coexpression modules. Coexpression analysis united genes expressed in drought‐stressed plants into nine modules covering 72 hub genes (87 hub isoforms), and genes expressed under controlled water conditions into 13 modules, covering 190 hub genes (251 hub isoforms). We find that low occupancy pan‐genes are under‐represented among several modules, while other modules are over‐enriched for low‐occupancy pan‐genes. We also provide new insight into the regulation of drought response inB. distachyon , specifically identifying one module with an apparent role in primary metabolism that is strongly responsive to drought. Our work shows the power of integrating pan‐genomic analysis with transcriptomic data using factorial experiments to understand the functional genomics of environmental response.