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1. Endosperm-based incompatibilities in hybrid monkeyflowers

   https://doi.org/10.1093/plcell/koab117  

   Kinser, Taliesin J.; Smith, Ronald D.; Lawrence, Amelia H.; Cooley, Arielle M.; Vallejo-Marín, Mario; Conradi Smith, Gregory D.; Puzey, Joshua R. (April 2021, The Plant Cell)

   Abstract Endosperm is an angiosperm innovation central to their reproduction whose development, and thus seed viability, is controlled by genomic imprinting, where expression from certain genes is parent-specific. Unsuccessful imprinting has been linked to failed inter-specific and inter-ploidy hybridization. Despite their importance in plant speciation, the underlying mechanisms behind these endosperm-based barriers remain poorly understood. Here, we describe one such barrier between diploid Mimulus guttatus and tetraploid Mimulus luteus. The two parents differ in endosperm DNA methylation, expression dynamics, and imprinted genes. Hybrid seeds suffer from underdeveloped endosperm, reducing viability, or arrested endosperm and seed abortion when M. guttatus or M. luteus is seed parent, respectively, and transgressive methylation and expression patterns emerge. The two inherited M. luteus subgenomes, genetically distinct but epigenetically similar, are expressionally dominant over the M. guttatus genome in hybrid embryos and especially their endosperm, where paternal imprints are perturbed. In aborted seeds, de novo methylation is inhibited, potentially owing to incompatible paternal instructions of imbalanced dosage from M. guttatus imprints. We suggest that diverged epigenetic/regulatory landscapes between parental genomes induce epigenetic repatterning and global shifts in expression, which, in endosperm, may uniquely facilitate incompatible interactions between divergent imprinting schemes, potentially driving rapid barriers. 

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2. Identification and analysis of imprinted genes in wild strawberry uncover a regulatory pathway in endosperm development

   https://doi.org/10.1093/plphys/kiae496  

   Joldersma, Dirk; Guo, Lei; Alger, Elizabeth I; Ippoliti, Christina; Luo, Xi; Platts, Adrian E; Edger, Patrick P; Liu, Zhongchi (September 2024, Plant Physiology)

   Abstract Fertilization is a fundamental process that triggers seed and fruit development, but the molecular mechanisms underlying fertilization-induced seed development are poorly understood. Previous research has established AGamous-Like62 (AGL62) activation and auxin biosynthesis in the endosperm as key events following fertilization in Arabidopsis (Arabidopsis thaliana) and wild strawberry (Fragaria vesca). To test the hypothesis that epigenetic mechanisms are critical in mediating the effect of fertilization on the activation of AGL62 and auxin biosynthesis in the endosperm, we first identified and analyzed imprinted genes from the endosperm of wild strawberries. We isolated endosperm tissues from F1 seeds of 2 wild strawberry F. vesca subspecies, generated endosperm-enriched transcriptomes, and identified candidate Maternally Expressed and Paternally Expressed Genes (MEGs and PEGs). Through bioinformatic analyses, we identified 4 imprinted genes that may be involved in regulating the expression of FveAGL62 and auxin biosynthesis genes. We conducted functional analysis of a maternally expressed gene FveMYB98 through CRISPR-knockout and over-expression in transgenic strawberries as well as analysis in heterologous systems. FveMYB98 directly repressed FveAGL62 at stage 3 endosperm, which likely serves to limit auxin synthesis and endosperm proliferation. These results provide an inroad into the regulation of early-stage seed development by imprinted genes in strawberries, suggest the potential function of imprinted genes in parental conflict, and identify FveMYB98 as a regulator of a key transition point in endosperm development. 

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3. The transcriptome landscape of developing barley seeds

   https://doi.org/10.1093/plcell/koae095  

   Kovacik, Martin; Nowicka, Anna; Zwyrtková, Jana; Strejčková, Beáta; Vardanega, Isaia; Esteban, Eddi; Pasha, Asher; Kaduchová, Kateřina; Krautsova, Maryna; Červenková, Marie; et al (April 2024, The Plant Cell)

   Abstract Cereal grains are an important source of food and feed. To provide comprehensive spatiotemporal information about biological processes in developing seeds of cultivated barley (Hordeum vulgare L. subsp. vulgare), we performed a transcriptomic study of the embryo, endosperm, and seed maternal tissues collected from grains 4–32 days after pollination. Weighted gene co-expression network and motif enrichment analyses identified specific groups of genes and transcription factors (TFs) potentially regulating barley seed tissue development. We defined a set of tissue-specific marker genes and families of TFs for functional studies of the pathways controlling barley grain development. Assessing selected groups of chromatin regulators revealed that epigenetic processes are highly dynamic and likely play a major role during barley endosperm development. The repressive H3K27me3 modification is globally reduced in endosperm tissues and at specific genes related to development and storage compounds. Altogether, this atlas uncovers the complexity of developmentally regulated gene expression in developing barley grains. 

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4. Imprinting and DNA Methylation in Water Lily Endosperm: Implications for Seed Evolution

   https://doi.org/10.1093/molbev/msaf271  

   Povilus, Rebecca A; Martin, Caroline A; Bechen, Lindsey L; Gehring, Mary (October 2025, Molecular Biology and Evolution)

   Larracuente, Amanda (Ed.)

   Abstract Endosperm is a key evolutionary innovation associated with the origin of angiosperms (flowering plants). This altruistic seed tissue supports the growth and development of the embryo by mediating the relationship of the mother plant as a nutrient source to the compatriot embryo as a nutrient sink. The endosperm is the primary site of gene imprinting in plants (where expression of an allele in offspring depends on which parent it was inherited from) and of parent-specific epigenetic modifications like DNA methylation, which are differentially patterned during male and female gamete development. Experimental results from a phylogenetically wide array of monocot and eudicot plants suggest these parent-of-origin effects are a common feature across angiosperms. However, information about genomic imprinting and epigenetic modifications in seeds of angiosperm lineages whose origins predate the monocot–eudicot divergence (such as Nymphaeales, water lilies) is extremely limited. Additionally, Nymphaeales are an intriguing lineage in which to investigate seed genetic and epigenetic phenomena, as they are characterized by diploid endosperm and a maternal storage tissue (perisperm), both of which are unusual across angiosperm diversity. Here, we examined DNA methylation and gene imprinting using two reproductively compatible water lily sister species, Nymphaea thermarum and Nymphaea dimorpha. Our results suggest that maternally expressed imprinted genes and differential DNA methylation of maternally and paternally inherited endosperm genomes are an ancestral condition for endosperm, whereas other seed characters like seed provisioning strategies, endosperm ploidy, and paternally expressed imprinted genes might have evolved as coinciding, opposing strategies in the evolutionary dialogue over parental control of offspring development. 

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5. Ancestral function but divergent epigenetic regulation of HAIKU2 reveals routes of seed developmental evolution

   https://doi.org/10.1016/j.molp.2022.09.002  

   Wu, D. (October 2022, Molecular Plant)

   Evolution is driven by various mechanisms. A directional increase in the embryo to endosperm ratio is an evolutionary trend within the angiosperms. The endosperm constitutes a major portion of the seed volume in Poales and some dicots. However, in other dicots such as Arabidopsis and soybean, the endosperm proliferates early, followed by embryo growth to replace the endosperm. The Arabidopsis leucine-rich repeat receptor protein kinase AtHAIKU2 (AtIKU2) is a key regulator of early endosperm proliferation. In this study, we found that IKU2s from Brachypodium, rice, and soybean can complement the abnormal seed developmental phenotype of Atiku2, while AtIKU2 also rescues the defective endosperm proliferation in the Brachypodium BdIKU2 knockout mutant seeds. AtIKU2 and soybean GmIKU2 are actively expressed a few days after fertilization. Thereafter, expression of AtIKU2 is suppressed by the FIS-PRC2 complex-mediated H3K27me3. The soybean GmIKU2 locus is also enriched with H3K27me3 marks. The histone methyltransferase AtMEA is unique to Brassicaceae, but one GmSWN in soybean plays a similar role in seed development as AtMEA. By contrast, the BdIKU2 and rice OsIKU2 loci are continuously expressed and are devoid of H3K27me3 marks. Taken together, these results suggest that IKU2 genes retain an ancestral function, but the duration of their expression that is controlled by PRC2-mediated epigenetic silencing contributes to silenced or persistent endosperm proliferation in different species. Our study reveals an epigenetic mechanism that drives the development of vastly different seed ontogenies. 

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