ORIGINAL RESEARCH article
Front. Plant Sci.
Sec. Plant Development and EvoDevo
Volume 16 - 2025 | doi: 10.3389/fpls.2025.1698577
Parent-of-origin effects orchestrate transcriptional reprogramming and epigenetic regulation of seedling vigor heterosis in triploid loquat
Provisionally accepted
- Southwest University, Chongqing, China
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Triploid breeding is a promising avenue for generating seedless varieties with enhanced vigor, yet the underlying molecular mechanisms, particularly the relative contributions of hybridity, ploidy level, and parent-of-origin effects (POE), remain largely elusive in perennial fruit crops. This study focuses on loquat (Eriobotrya japonica), a highly heterozygous woody perennial, to explore the molecular mechanism of triploid seedling vigor heterosis. RNA-seq across a series of reciprocal diploid (2x), triploid (3x) and tetraploid (4x) hybrids with clear genetic background revealed POE as the predominant driver of triploid heterosis at the transcriptomic level. Specifically, 784 POE-responsive differentially expressed genes (DEGs) were identified between paternal-excess [3x(p)] and maternal-excess [3x(m)] triploids, exceeding the effects of ploidy (218-652 DEGs) and hybridity (8-90 DEGs). For an in-depth investigation, reciprocal crosses between L2 and L4 were further selected for an integrated transcriptome, allele-specific expression (ASE), and allele-specific methylation (ASM) analysis. Our findings demonstrate that POE orchestrates multilayered regulation, including (i) coordinated upregulation of vigor-related pathways (i.e., photosynthesis, starch metabolism, plant circadian rhythm) in 3x(p); (ii) a dual ASE pattern with maternal bias in gene quantity but paternal enhancement in levels, including five paternally expressed imprinted genes (PEGs); (iii) nonclassical epigenetic regulation where paternal gene body hypermethylation (mCG) paradoxically enhances transcription, especially in circadian clock genes. Finally, qRT-PCR-based diurnal expression across all crosses validated that POE-dependent reprogramming of key circadian oscillator genes (EjCCA1, EjLHY, EjGI, EjTOC1), suggesting optimized metabolic efficiency through circadian clock modulation might contribute to enhanced vigor in 3x(p) hybrids. This study provides fundamental insights into the dosage-sensitive gene networks and epigenetic regulation underlying POE-driven heterosis in woody perennials, advancing polyploid heterosis theory and offering novel targets for genetic improvement.
Keywords: Loquat, triploid heterosis, parent-of-origin effects, allele-specific expression, allele-specific methylation, Circadian clock, woody perennial
Received: 03 Sep 2025; Accepted: 30 Sep 2025.
Copyright: © 2025 Zhang, Yuan, Guo, Dang, Liang, Gou, Guo and Wu. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
* Correspondence:
Qigao Guo, qgguo@126.com
Di Wu, wudisuper610@126.com
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