Chromosome doubling is associated with enhanced self-compatibility and transcriptional remodeling of pollen-pistil interactions in Lycium chinense.

Abstract

Key message: Cytology and 72-sample pistil transcriptomes link chromosome doubling to self-compatibility in autotetraploid Lycium chinense through altered pollen-pistil responses and candidate S-RNase trafficking and detoxification pathways. Polyploidy can reshape plant reproductive traits and self-compatibility systems, yet the mechanisms underlying ploidy-associated transitions to self-compatibility remain poorly understood. In this study, diploid and autotetraploid Lycium chinense were compared using floral morphology, stigma receptivity, pollen viability, and pollen tube cytology, controlled pollination, seed vigor analysis, and transcriptome sequencing of 72 pistil samples spanning stigma, style, and ovary tissues at four pollination stages. Chromosome doubling enlarged reproductive organs, prolonged stigma receptivity, and increased pollen size, while also altering pollen performance and pollen tube growth. Diploid self-pollen tubes were arrested in the upper style, whereas autotetraploid self-pollen tubes continued through the style, accompanied by a marked increase in self-compatibility, with the compatibility index rising from 0.50 to 5.70 and fruit set from 8.33% to 73.33%. Spatiotemporal transcriptome analysis revealed extensive tissue- and time-dependent transcriptional remodeling between ploidy levels. Temporal clustering and ploidy × time interaction analyses showed particularly pronounced divergence in the stigma and style, with the style exhibiting the strongest interaction response. WGCNA further identified tissue-associated co-expression modules enriched in membrane trafficking, phosphatidylinositol signaling, endocytosis, SNARE-mediated vesicular transport, and ubiquitin-mediated protein turnover. Reported GSI-related homologs, including LcS-RNase, LcHT-B, Lc120K, LcStEP, LcSBP1, and LcSKP1, also displayed distinct spatiotemporal expression patterns. Integrating these observations, we propose a working model in which heteroallelic pollen effects, altered S-RNase compartmentalization, and protein turnover may jointly reduce S-RNase-mediated cytotoxicity and permit continued self-pollen tube growth in autotetraploid L. chinense. These findings provide a cytological and transcriptomic framework for understanding ploidy-associated GSI breakdown and its potential relevance to polyploid breeding in Lycium.