Rising global temperatures are altering soil ecosystems, influencing the distribution, fitness, and adaptive strategies of plant-parasitic nematodes, including Meloidogyne spp. Although Meloidogyne spp. exhibit considerable thermal plasticity, the molecular mechanisms underlying population-specific adaptation remain unclear. This study investigates the phenotypic and transcriptomic responses to heat stress in three geographically distinct Meloidogyne incognita populations, Arava (hot desert), Jordan Valley (JV) (semiarid), and Carmel (temperate), under controlled soil temperatures (25 °C, 30 °C, 33 °C). Infection-induced phenotypic responses, including galling index, plant growth, and egg production, were evaluated, while RNA sequencing enabled differential gene-expression analysis, KEGG pathway enrichment, and protein–protein interaction (PPI) network mapping. The Arava population, preadapted to high temperatures, maintained peak egg production (633.86 % and 178.7 % increase at 30 °C and 33 °C, respectively) with minimal transcriptomic shifts, selective activation of small heat shock proteins (sHSPs) and glycerolipid metabolism, ensuring energy-efficient resilience at 33 °C. In contrast, the Carmel population displayed a sharp decline in egg production by 78.8 % at 33 °C, and extreme transcriptomic plasticity at 33 °C, with 6860 differentially expressed genes, including upregulation of 89 oxidative phosphorylation, 55 arginine/proline metabolism, and 32 glutathione metabolism genes, indicating a fitness trade-off between stress response and reproductive success. The JV population exhibited an intermediate adaptive strategy, with a 243.2 % increase in egg production at 30 °C but only a 6.48 % increase at 33 °C, with increased pathways of balancing autophagy, DNA repair, and metabolic adjustments. KEGG pathway analysis revealed population-specific metabolic trade-offs, whereas PPI networks showed distinct HSP clustering in Carmel, contrasting with Arava’s streamlined, energy-efficient response. We show M. incognita populations’ distinct adaptive strategies under thermal stress—preadaptation (Arava), transcriptional reprogramming (Carmel), and balanced plasticity (JV), shaping their persistence under climate change. Preadapted populations are likely to expand into warmer regions, whereas plastic populations may experience fitness constraints under prolonged heat stress. These findings provide a predictive framework for nematode-range shifts and highlight the need to integrate molecular stress responses into pest-risk models to develop climate-resilient nematode-management strategies.
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