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Review
. 2024 Apr 30;195(1):155-169.
doi: 10.1093/plphys/kiae050.

Molecular basis and evolutionary drivers of endosperm-based hybridization barriers

Heinrich Bente  1 , Claudia Köhler  1   2
Affiliations
Review

Molecular basis and evolutionary drivers of endosperm-based hybridization barriers

Heinrich Bente et al. Plant Physiol. .

Abstract

The endosperm, a transient seed tissue, plays a pivotal role in supporting embryo growth and germination. This unique feature sets flowering plants apart from gymnosperms, marking an evolutionary innovation in the world of seed-bearing plants. Nevertheless, the importance of the endosperm extends beyond its role in providing nutrients to the developing embryo by acting as a versatile protector, preventing hybridization events between distinct species and between individuals with different ploidy. This phenomenon centers on growth and differentiation of the endosperm and the speed at which both processes unfold. Emerging studies underscore the important role played by type I MADS-box transcription factors, including the paternally expressed gene PHERES1. These factors, along with downstream signaling pathways involving auxin and abscisic acid, are instrumental in regulating endosperm development and, consequently, the establishment of hybridization barriers. Moreover, mutations in various epigenetic regulators mitigate these barriers, unveiling a complex interplay of pathways involved in their formation. In this review, we discuss the molecular underpinnings of endosperm-based hybridization barriers and their evolutionary drivers.

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Conflict of interest statement

Conflict of interest statement. None declared.

Figures

Figure 1.
Figure 1.
Widespread occurrence of EBBs. The presence of endosperm corresponds closely with the emergence of robust hybridization barriers. In gymnosperms, embryo development is supported by the enlarged female gametophyte (denoted by parallel lines), whereas angiosperms have successfully integrated fertilization with the formation of a nourishing endosperm tissue. The endosperm may initiate as a cellular structure, as seen in ANA (Amborella, Nymphaeales, and Austrobaileyales) species that are sister lineages to all other angiosperms (indicated by the checkerboard pattern), or as a coenocyte where initial nuclear divisions are not synchronized with cellularization (depicted by the dotted pattern). References for each category of barriers are provided; for a more comprehensive exploration of reported barriers, we direct readers to Coughlan (2023). References in light green refer to barriers occurring in nuclear-type endosperm. Dark green references refer to cellular-type barriers. Checkmarks symbolize presence of EBBs. Brackets symbolize that insufficient data are available to determine whether the endosperm is affected in hybrid seeds. Question marks symbolize that no data are available yet.
Figure 2.
Figure 2.
Molecular pathways underlying endosperm-based interploidy and interspecies barriers. Maternal Pol IV–dependent siRNAs act as dosage-dependent repressors of AGL MADS-box genes. Increased dosage of siRNAs in maternal excess crosses corresponds with strong AGL repression (reflected by blunt-ended arrows; thickness of the arrows corresponds to intensity of repression) and early endosperm cellularization, while decreased siRNA dosage in paternal excess crosses corresponds with increased AGL abundance and late endosperm cellularization. High and low AGL dosage causes increased or decreased expression of downstream AGL targets, respectively, including auxin biosynthesis genes. Downstream direct or indirect targets of this signaling cascade are genes involved in pectin metabolism, including pectin methylesterase (PME) genes. Demethylesterification exposes pectin to pectin–degrading enzymes, thereby establishing a connection between the expression level of AGLs and the timing of endosperm cellularization. Abundance of AGLs and their downstream targets in response to hybridization are depicted by red (low), gray (balanced), and blue (high) arrows. Light and dark green endosperm regions mark micropylar and chalazal domains, respectively. ADM, ADMETOS; AGLs, AGAMOUS-LIKE genes; EBN, endosperm balance number; IKU2, HAIKU2; MINI3, MINISEED3; NRPD1, NUCLEAR RNA POLYMERASE D1; PEG2, PATERNALLY EXPRESSED GENE2; UBP1, OLIGOURIDYLATE BINDING PROTEIN 1B; PKR2, PICKLE RELATED2; SUVH7, SU(VAR)3–9 HOMOLOG 7; TAR1, TAA1-RELATED1; TEs, transposable elements; YUC10, YUCCA10.
Figure 3.
Figure 3.
Regulation of endosperm cellularization by antagonizing activities of auxin and ABA. ABA activates the downstream transcription factor ABI5, which, in turn, is stabilized by mobile factors such as TFL1, which is transported from the chalazal region to the peripheral endosperm. The mobilization of TFL1 is facilitated by RAN1. ABI5, under the influence of ABA, exerts its regulatory function by downregulating SHB1. SHB1 is a positive regulator of 2 critical genes, MINI3 and IKU2, both of which are direct targets of PHE1. MINI3 and IKU2 act as positive regulators of endosperm proliferation (symbolized by red dots). The repression of MINI3 and IKU2 via the ABA pathway likely promotes endosperm cellularization. Failure of endosperm cellularization can trigger an osmotic stress response in the embryo. Red arrows in this network represent the auxin-PHE1 pathway, and blue arrows highlight the ABA signaling pathway. Upward-pointing arrows reflect increased expression or activity, while downward-pointing arrows reflect decreased expression or activity. Arrows with blunt ends reflect repressive activity. Light and dark green endosperm regions mark micropylar and chalazal domains, respectively. ABI5, ABSCISIC ACID-INSENSITIVE5; IKU2, HAIKU2; MINI3, MINISEED3; PHE1, PHERES1; RAN1, Ras-related nuclear GTPase1; SHB1, SHORT HYPOCOTYL UNDER BLUE1; TFL1, TERMINAL FLOWER1.
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