Similarities between Reproductive and Immune Pistil Transcriptomes of Arabidopsis Species

Abstract

ORCID IDs: 0000-0002-9468-6335 (M.M.-P.); 0000-0001-6442-4302 (T.D.).Independent lines of evidence suggest that members from ancient and polymorphic gene families such as defensins and receptor-like kinases mediate intercellular communication during both the immune response and reproduction. Here, we report a large-scale analysis to investigate the extent of overlap between these processes by comparing differentially expressed genes (DEGs) in the pistil transcriptomes of Arabidopsis thaliana and Arabidopsis halleri during self-pollination and interspecific pollination and during infection with Fusarium graminearum. In both Arabidopsis species, the largest number of DEGs was identified in infected pistils, where genes encoding regulators of cell division and development were most frequently downregulated. Comparison of DEGs between infection and various pollination conditions showed that up to 79% of down-regulated genes are shared between conditions and include especially defensin-like genes. Interspecific pollination of A. thaliana significantly up-regulated thionins and defensins. The significant overrepresentation of similar groups of DEGs in the transcriptomes of reproductive and immune responses of the pistil makes it a prime system in which to study the consequences of plantpathogen interactions on fertility and the evolution of intercellular communication in pollination.

Diversification of defensins and NLRs in Arabidopsis species by different evolutionary mechanisms

“…As a control, pistils collected 24 h after emasculation, but otherwise untreated, were used for comparison with infected pistils. The surface of infected pistils and leaves collected 3 days after infection (3 DAI) showed profuse hyphal growth in A. lyrata (Additional file 8 : Figure S3) as well as in A. thaliana and A. halleri [ 20 ]. For both control and treatments, pistils or leaves from three biological replicates were collected, each replicate containing equivalent amounts of material from 4 individual plants.…”

“…For example, DEFL SCRs are involved in self-incompatibility [ 18 ], while LUREs, another DEFL subgroup, are secreted by ovules to attract competent pollen tubes of their own species during pollination [ 19 ]. Many DEFLs of these and other subgroups are differentially expressed also in the immune responses to Fusarium graminearum [ 20 ]. Similarly, the Capsicum annum defensin CADEF1 is expressed in response to both biotic and abiotic stresses [ 21 ] while antimicrobial PDF1s form Arabidopsis thaliana more closely related to DEFLs that confer heavy metal tolerance in Arabidopsis halleri [ 22 ].…”

“…We tested the contribution of transcriptional divergence to the evolution of both families by characterizing their expression in pistils and leaves infected with Fusarium graminearum , a heterotrophic flower-infecting fungus responsible for cereal head blight. This approach was based on the finding that DEFLs are predominantly expressed in reproductive tissues [ 29 ] as well as in response to pathogens and pollination [ 20 ].…”

The molecular signatures of compatible and incompatible pollination

“…The similarity between the stigma-pollen interaction and plant-pathogen interaction has been discussed and has drawn researchers’ attention for a long time 10,42–44 . Several transcriptomic analyses of pollinated stigmas/pistils reported enrichment in transcripts linked to stress or defense response in female tissues 18,20,33,44,45 . Tung et al and Leydon et al suggested that such defense-related genes would have function in pollination.…”

“…Tung et al and Leydon et al suggested that such defense-related genes would have function in pollination. Moreover, the incompatible response has been considered to share common mechanism with plant-pathogen interaction as it is a response to block the invader 18,44 . However, in our analysis, GO terms associated with defense responses did not clearly appear after incompatible pollination but rather were mainly represented in compatible response (Fig.…”