Differences in Effective Ploidy Drive Genome-Wide Endosperm Expression Polarization and Seed Failure in Wild Tomato Hybrids

Abstract

Parental imbalances in the endosperm leading to impaired development and eventual hybrid seed failure are common causes of postzygotic isolation in flowering plants. Endosperm sensitivity to parental dosage is reflected by canonical phenotypes of “parental excess” in reciprocal interploid crosses. Moreover, parental-excess traits are also evident in many homoploid interspecific crosses, potentially reflecting among-lineage variation in “effective ploidy” driven by endosperm properties. However, the genetic basis of effective ploidy is unknown and genome-wide expression perturbations in parental-excess endosperms from homoploid crosses have yet to be reported. The tomato clade (Solanum section Lycopersicon), encompassing closely related diploids with partial-to-complete hybrid seed failure, provides outstanding opportunities to study these issues. Here, we compared replicated endosperm transcriptomes from six crosses within and among three wild tomato lineages. Strikingly, strongly inviable hybrid crosses displayed conspicuous, asymmetric expression perturbations that mirror previously characterized parental-excess phenotypes. Solanum peruvianum, the species inferred to have evolved higher effective ploidy than the other two, drove expression landscape polarization between maternal and paternal roles. This global expression divergence was mirrored in functionally important gene families such as MADS-box transcription factors and E3 ubiquitin ligases, and revealed differences in cell cycle tuning that match phenotypic differences in developing endosperm and mature seed size between reciprocal crosses. Our work starts to uncover the complex interactions between expression divergence, parental conflict, and hybrid seed failure that likely contributed to plant diversity.

Endosperm and seed transcriptomes reveal possible roles for small RNA pathways in wild tomato hybrid seed failure

“…We interpret the pattern of S. peruvianum dominance as consistent with the rationale of the weak inbreeder/strong outbreeder (WISO) hypothesis (Brandvain and Haig 2005), with the S. peruvianum genome ‘overpowering’ that of S. chilense , which putatively evolved under lower levels of parental conflict. These inferences are in accordance with our prior and current evidence for higher effective ploidy of S. peruvianum compared to S. chilense (Roth et al 2019), and how it plausibly underpins seeds’ developmental and phenotypic differences between these two wild tomato lineages: smaller hybrid seed size and transcriptomic signals (Florez-Rueda, Paris, et al 2016; Roth, Florez-Rueda, Griesser, et al 2018; Roth et al 2019), such as a higher proportion of DE genes, DE sRNAs, and larger shifts toward maternal allelic expression in PC (compared to CP) hybrid endosperm.…”

“…MADS-domain TFs have been shown to play key regulatory roles in plant reproduction, in particular in regulating female gametophyte, embryo, and endosperm development (reviewed in Masiero et al 2011). Likewise, AGAMOUS-LIKE ( AGL ) genes were jointly overexpressed in ‘paternal-excess-like’ crosses involving S. chilense , S. peruvianum , and S. arcanum (Roth et al 2019). These TFs are part of the GO protein dimerization activity (GO:0046983) and include 11 AGL genes, 13 2FE-2S FERREDOXIN-LIKE genes, three PHERES genes, APETALLA3 and SEPALATA3 , among others (supplementary tables S3, S6, Supplementary Material online).…”

“…Likewise, S. peruvianum drives expression landscape polarization in hybrid endosperms derived from reciprocal crosses with S. chilense and S. arcanum (Roth et al 2019). In line with these observations, our analyses of the expression modes of DE sRNAs and genes revealed a trend of S. peruvianum dominance in CP hybrid seeds and endosperm, respectively (figure 5C, D, upper panel).…”

A high maternal genome excess causes severe seed abortion leading to ovary abscission in Nicotiana interploidy‐interspecific crosses

“…Surprisingly, when we increased N. tabacum ploidy, type II seed abortion was prevented, leading to suppression of another postzygotic reproductive barrier-ovary abscission. This is likely due to the direct relationship between type II seed abortion and ovary abscis- (Coughlan et al, 2020;Lafon-Placette et al, 2018;Roth et al, 2019;). In the present study, we can infer that the relative effective ploidies between N. suaveolens accessions are PI 555565 (8x) ≈ PI 555561 (16x)> PI 555561 (8x) ≈ PI 555568 (8x)> PI 555568 (4x).…”

“…The abnormal endosperm development in interspecific crosses between species with the same ploidy level can be bypassed by changing the ploidy of one parental species (Bushell et al, 2003;Johnston and Hanneman, 1982;Lafon-Placette et al, 2017;Tonosaki et al, 2018). Moreover, genome-wide studies on endosperm gene expression have revealed that genomic imprinting is extensively perturbed in failing hybrid endosperm in Solanum, Capsella and several other species (Lafon-Placette et al, 2018;Roth et al, 2019;Tonosaki et al, 2018).…”