A slow-then-rapid spike development trajectory enables wheat to escape late-spring cold spells via transcriptional...

Late-spring cold spells (LSCs) threaten bread wheat (Triticum aestivum L.) when cold-sensitive spike development coincides with ephemeral spring chilling. The leading Chinese cultivar Xinong 511 (XN511) exhibits superior LSC tolerance, yet the underlying developmental and molecular basis remains unclear. Phenotypic monitoring across eight sequential sampling points, designated T1-T8, revealed that XN511 displays a distinctive "slow-then-rapid" developmental trajectory relative to its parents, Xinong 2000 (XN2000) and Shaanmai 159 (SM159): an extended early vegetative phase followed by accelerated late-stage progression. This unique pattern enables temporal avoidance of the historical LSC peak window in the Yellow-Huai River Valley. To dissect the genetic circuitry, we performed time-course RNA sequencing (RNA-seq) across T1-T8, which identified 15,440 dynamically expressed genes and pinpointed T2 and T5 as two pivotal phase-transition checkpoints. Guided by these transcriptomic landmarks, we conducted whole-genome bisulfite sequencing (WGBS) precisely at T2 and T5. WGBS revealed stage-specific methylation reprogramming, identifying 172 differentially methylated regions (DMR)-associated differentially expressed genes (DEGs) at T2 and 560 at T5, including TaLNK2-3B, TaACS6-5B, and TaAP3-7D. Functional enrichment identified the SPL-AP2L aging/phase-transition pathway as a core transcriptional hub, with AP2L expression sustained longer and SPL activation delayed in XN511 relative to its parents. Collectively, our findings establish a multi-layered regulatory framework, which integrates transcriptional timing with stage-specific epigenetic reprogramming, that underpins the adaptive developmental strategy of XN511, providing both genetic and epigenetic targets for breeding wheat cultivars with improved resilience to LSCs.