Novel allelic variants in ACD6 cause hybrid necrosis in local collection of Arabidopsis thaliana

Abstract

Hybrid necrosis is a common type of hybrid incompatibility in plants. This phenomenon is caused by deleterious epistatic interactions, resulting in spontaneous activation of plant defenses associated with leaf necrosis, stunted growth and reduced fertility in hybrids. Specific combinations of alleles of ACCELERATED CELL DEATH 6 (ACD6) have been shown to be a common cause of hybrid necrosis in Arabidopsis thaliana. Increased ACD6 activity confers broad-spectrum resistance against biotrophic pathogens but reduces biomass production. We generated 996 crosses among individuals derived from a single collection area around Tübingen (Germany) and screened them for hybrid necrosis. Necrotic hybrids were further investigated by genetic linkage, amiRNA silencing, genomic complementation and metabolic profiling. Restriction site associated DNA (RAD)-sequencing was used to understand genetic diversity in the collection sites containing necrosis-inducing alleles. Novel combinations of ACD6 alleles found in neighbouring stands were found to activate the A. thaliana immune system. In contrast to what we observed in controlled conditions, necrotic hybrids did not show reduced fitness in the field. Metabolic profiling revealed changes associated with the activation of the immune system in ACD6-dependent hybrid necrosis. This study expands our current understanding of the active role of ACD6 in mediating trade-offs between defense responses and growth in A. thaliana.

Plasticity in metabolism underpins local responses to nitrogen in Arabidopsis thaliana populations

“…Fifteen individual plants collected from Lövvik (Lov), Northern Sweden in year 2015 (Plotner et al, ), and 15 individual plants from Altenriet (Alt), Southern Germany in 2013 (Swiadek et al, ), were used in this study. In all conditions, soil contained 50% (v/v) fine white peat (Gramoflor GmbH) mixed with 30% (v/v) fine and 25% (v/v) coarse‐grained vermiculite peat (Fitz Kausek GmbH & Co).…”

“…To test the hypothesis, we analyzed plasticity to N availability in 65 primary metabolites as well as growth and fitness traits in two A. thaliana populations, one collected from Southern Germany and the other from Northern Sweden. These populations originate from different growth habitats and differ genetically (Plotner et al, ; Swiadek et al, ). Interestingly, we found that glutamine, an amino acid central to the assimilation of N, exhibited the highest plasticity in both populations.…”

Diverse paths to hybrid incompatibility in Arabidopsis

“…Although the most severe cases of F 1 hybrid necrosis are lethal, the milder cases are partially fertile or have phenotypes that become visible only in the F 2 or later generations. All cases of hybrid necrosis show phenotypic characteristics typical of the defense response to pathogens in plants (Bomblies et al ., ; Alcázar et al ., , , ; Chae et al ., ; Todesco et al ., ; Swiadek et al ., ). The first causal gene pair underlying hybrid necrosis was identified from A. thaliana (Bomblies et al ., ).…”

“…In contrast to the NLR s, where phenotypes result from an interaction between two or three different genes, interactions between different allelic variants of ACD6 can activate autoimmune responses in F 1 hybrids of A. thaliana (Todesco et al ., ; Swiadek et al ., ). Furthermore, interactions of different ACD6 alleles have been shown to cause different severity of symptoms in A. thaliana hybrids (Todesco et al ., ; Swiadek et al ., ). Although showing reduced fitness, these hybrids also display an increased disease resistance in comparison with their parents (Todesco et al ., ).…”

“…For the sequenced A. thaliana accessions, transcriptome and epigenome resources are also publically available (Kawakatsu et al ., ; http://neomorph.salk.edu/1001.aj.php). In addition to these resources, SNP genotyping using the restriction site associated DNA sequencing (RADseq) technique, allowing high‐density single‐nucleotide polymorphism (SNP) genotyping of thousands of individuals in a cost‐effective way (Davey et al ., ; Arnold et al ., ), has been applied to several species in the Arabidopsis genus (Todesco et al ., ; Buckley et al ., ; Jiang et al ., ; Kolář et al ., ; Fischer et al ., ; Swiadek et al ., ; Fan et al ., ). These genetic resources have not only improved the power of genome‐wide association (GWA) studies and quantitative trait locus (QTL) mapping, which are used to identify genes underlying adaptive traits in plants, but they have also allowed the study of evolution by comparison and analysis of genome sequences within and between individuals of the same and closely related species.…”