Heritable differences in abundance of bacterial rhizosphere taxa are correlated with fungal necrotrophic pathogen resistance.

Host-microbe interactions are increasingly recognized as important drivers of organismal health, growth, longevity and community-scale ecological processes. However, less is known about how genetic variation affects hosts' associated microbiomes and downstream phenotypes. We demonstrate that sunflower (Helianthus annuus) harbours substantial, heritable variation in microbial communities under field conditions. We show that microbial communities co-vary with heritable variation in resistance to root infection caused by the necrotrophic pathogen Sclerotinia sclerotiorum and that plants grown in autoclaved soil showed almost complete elimination of pathogen resistance. Association mapping suggests at least 59 genetic locations with effects on both microbial relative abundance and Sclerotinia resistance. Although the genetic architecture appears quantitative, we have elucidated previously unexplained genetic variation for resistance to this pathogen. We identify new targets for plant breeding and demonstrate the potential for heritable microbial associations to play important roles in defence in natural and human-altered environments.

Genetic loci underlying quantitative resistance to necrotrophic pathogens Sclerotinia and Diaporthe (Phomopsis), and correlated resistance to both pathogens.

KEY MESSAGE: We provide results rooted in quantitative genetics, which combined with knowledge of candidate gene function, helps us to better understand the resistance to two major necrotrophic pathogens of sunflower. Necrotrophic pathogens can avoid or even benefit from plant defenses used against biotrophic pathogens, and thus represent a distinct challenge to plant populations in natural and agricultural systems. Sclerotinia and Phomopsis/Diaporthe are detrimental pathogens for many dicotyledonous plants, including many economically important plants. With no well-established methods to prevent infection in susceptible plants, host-plant resistance is currently the most effective strategy. Despite knowledge of a moderate, positive correlation in resistance to the two diseases in sunflower, detailed analysis of the genetics, in the same populations, has not been conducted. We present results of genome-wide analysis of resistance to both pathogens in a diversity panel of 218 domesticated sunflower genotypes of worldwide origin. We identified 14 Sclerotinia head rot and 7 Phomopsis stem canker unique QTLs, plus 1 co-located QTL for both traits, and observed extensive patterns of linkage disequilibrium between sites for both traits. Most QTLs contained one credible candidate gene, and gene families were common for the two disease resistance traits. These results suggest there has been strong, simultaneous selection for resistance to these two diseases and that a generalized mechanism for defense against these necrotrophic pathogens exists.

Genetics of alternative splicing evolution during sunflower domestication.

Alternative splicing enables organisms to produce the diversity of proteins necessary for multicellular life by using relatively few protein-coding genes. Although differences in splicing have been identified among divergent taxa, the shorter-term evolution of splicing is understudied. The origins of novel splice forms, and the contributions of alternative splicing to major evolutionary transitions, are largely unknown. This study used transcriptomes of wild and domesticated sunflowers to examine splice differentiation and regulation during domestication. We identified substantial splicing divergence between wild and domesticated sunflowers, mainly in the form of intron retention. Transcripts with divergent splicing were enriched for seed-development functions, suggesting that artificial selection impacted splicing patterns. Mapping of quantitative trait loci (QTLs) associated with 144 differential splicing cases revealed primarily trans-acting variation affecting splicing patterns. A large proportion of identified QTLs contain known spliceosome proteins and are associated with splicing variation in multiple genes. Examining a broader set of wild and domesticated sunflower genotypes revealed that most differential splicing patterns in domesticated sunflowers likely arose from standing variation in wild Helianthus annuus and gained frequency during the domestication process. However, several domesticate-associated splicing patterns appear to be introgressed from other Helianthus species. These results suggest that sunflower domestication involved selection on pleiotropic regulatory alleles. More generally, our findings indicate that substantial differences in isoform abundances arose rapidly during a recent evolutionary transition and appear to contribute to adaptation and population divergence.