Early Disruption of Maternal–Zygotic Interaction and Activation of Defense-Like Responses inArabidopsisInterspecific Crosses    

Abstract

Seed death resulting from hybridization between Arabidopsis thaliana and Arabidopsis arenosa has complex genetic determination and involves deregulation 5 to 8 d after pollination (DAP) of AGAMOUS-LIKE genes and retroelements. To identify causal mechanisms, we compared transcriptomes of compatible and incompatible hybrids and parents at 3 DAP. Hybrids misexpressed endosperm and seed coat regulators and hyperactivated genes encoding ribosomal, photosynthetic, stress-related, and immune response proteins. Regulatory disruption was more severe in Columbia-0 hybrids than in C24 hybrids, consistent with the degree of incompatibility. Maternal loss-of-function alleles for endosperm growth factor TRANSPARENT TESTA GLABRA2 and HAIKU1 and defense response regulators NON-EXPRESSOR OF PATHOGENESIS RELATED1 and SALICYLIC ACID INDUCTION-DEFICIENT2 increased hybrid seed survival. The activation of presumed POLYCOMB REPRESSIVE COMPLEX (PRC) targets, together with a 20-fold reduction in expression of FERTILIZATION INDEPENDENT SEED2, indicated a PRC role. Proximity to transposable elements affected natural variation for gene regulation, but transposon activation did not differ from controls. Collectively, this investigation provides candidates for multigenic orchestration of the incompatibility response through disruption of endosperm development, a novel role for communication between endosperm and maternal tissues and for pathways previously connected to immunity, but, surprisingly, does not identify a role for transposons.

Hypomethylated Pollen Bypasses the Interploidy Hybridization Barrier inArabidopsis

“…Expression of FIS-PRC2 subunit encoding genes MEDEA (MEA) and FIS2 was suppressed by met1 and osd1 met1 pollen, suggesting that normalization of triploid seed development by osd1 met1 pollen is not a consequence of normalized MEA and FIS2 expression. Mutants in NONEXPRESSOR OF PR GENES (NPR1) and SALICYLIC ACID INDUCTION-DEFICIENT2 (SID2) were previously shown to suppress hybrid seed abortion (Burkart-Waco et al, 2013). However, expression of NPR1 was further increased in osd1 met1 and met1 derived seeds compared with osd1 and wild-type pollinated controls, while expression of SID2 was largely unchanged in the corresponding crosses, suggesting that both genes are unlikely to play a causal role in restoring triploid seed rescue.…”

“…We specifically analyzed genes that were previously shown to be deregulated in triploid seeds and in interspecific hybrid seeds (Tiwari et al, 2010;Burkart-Waco et al, 2013;Kradolfer et al, 2013b) (Supplemental Figure 3). Expression of all analyzed type I MADS box transcription factor genes, as well as HAIKU genes (IKU1 and IKU2) and TRANSPARENT TESTA GLABRA2, was suppressed by osd1 met1 pollen, consistent with a normalization of triploid seed development.…”

Hormone-regulated defense and stress response networks contribute to heterosis inArabidopsisF1 hybrids

“…Elevated SA response, changes in auxin concentrations, increased defense gene expression, and reduced growth parameters all occur in a less frequent hybridization outcome termed hybrid weakness (45,52,67,68), and at its extreme, hybrid incompatibility (69), providing additional support to the competitive interaction of defense pathways and growth regulation determining levels of heterosis. Hybrid vigor and hybrid weakness may represent opposite outcomes of changes to SA-and IAA-regulated pathways that are determined by interactions between defense and stress response allele and epiallele combinations provided through the cross to produce the hybrids.…”

Seed evolution: parental conflicts in a multi-generational household

“…This may be because maternal siRNAs are unable to repress the paternallyderived retrotransposons. However, other transposons than ATHILA do not appear to become activated in the A. thaliana x A. arenosa cross (116,133), suggesting that retrotransposon activation is not a general consequence of interspecific crosses.…”

“…The endosperm of seeds developing from maternal homozygous ttg2/ttg2 mutants cellularize precociously and seeds are small; however, maternal heterozygous ttg2/TTG2 mutants generate normal seeds, suggesting that TTG2 controls seed development as a maternal seed coat sporophytic factor, possibly by controlling integument cell elongation (138). Natural allelic variation at the TTG2 locus is also responsible for variation in the tolerance to interploidy crosses in Arabidopsis, and ttg2 mutants can reduce seed lethality in paternal excess and in interspecific crosses (133,139).…”