Heat acclimation induces AcLBD1 activated AcHSFA2s mutual amplification cascade for rapid recovery of root vitality and leaf photosynthesis in kiwifruit

Introduction Kiwifruit ( Actinidia spp.) is a succulent, shallow-rooted perennial fruit tree highly sensitive to environmental fluctuations, particularly the increasingly frequent extreme heat events. Methods This study investigated heat acclimation (HA) involving a transition from mild (35 °C) to extreme (45 °C) heat stress in heat-sensitive kiwifruit, aiming to elucidate the molecular biological mechanisms underlying HA responses in perennial plants. Results Results revealing the enhanced recovery of plants under 55 °C stress via improved root vitality and photosynthesis. Transcriptomics identified AcLBD1 as a key acclimation-responsive gene that upregulates AcHSFA2-1 . The achsfa2-1 loss-of-function mutant displayed completely impaired thermotolerance, with significantly suppressed expression of AcHSFA2-2 in its transcriptome. Overexpressing AcHSFA2-2 increased root vitality as high as 4.13‑fold and boosted post‑heat‑stress recovery of 35S:: AcHSFA2-2 kiwifruit. Moreover, AcHSFA2‑1 and AcHSFA2‑2 form a positive feedback loop, that AcHSFA2‑1 significantly enhanced the promoter vitality of AcHSFA2-2 , and vice versa. And the AcLBD1‑AcHSFA2s module co‑activates AcHSP20s encoding heat-protective proteins (with AcHSFA2s more potent than AcLBD1). Discussion These findings establish a LBD‑HSFA2‑HSP20 cascade network governing heat resilience via root and photosynthetic recovery, advancing the molecular basis of plant heat acclimation.