Climate-driven transcriptomic variation reveals population-specific adaptation strategies in geographically diverse Meloidogyne incognita populations

• As global temperatures rise, such localized adaptation strategies will likely influence the geographical distribution and agricultural impact of M. incognita populations. Climate change is expected to favor preadapted populations such as those in Arava, enabling range expansion into warmer regions, a trend already observed in M. incognita infestations in coffee plantations under warming climates ( Ghini et al., 2008 ). On the other hand, populations with high transcriptomic plasticity, such as that in Carmel, may undergo stress-induced range shifts, adapting to new climates but at potential fitness costs. Understanding these adaptation mechanisms is crucial for predicting nematode–host interactions and developing effective pest-management strategies under future climate scenarios. The integration of transcriptomic resilience into forecasting models can improve predictions of nematode outbreaks and range shifts. Similar approaches have been used to model the impact of climate change on gastrointestinal nematodes in livestock, demonstrating the relevance of climate-adaptive nematode management (Fox et al., 2022). Future research should incorporate transcriptomic and ecological data into predictive models, allowing for proactive interventions to mitigate nematode-driven agricultural losses. Key findings of the Current Study: • The Arava RKN population exhibits a thermally preadapted state, characterized by minimal transcriptomic shifts at 33°C, targeted activation of basal stress pathways, reliance on glycerolipid metabolism, and a selective HSP response. Unlike the Carmel population, HSP activation in Arava RKNs follows an energy-efficient strategy, ensuring stable reproductive success under high temperatures. • The Carmel population demonstrates high transcriptomic plasticity, undergoing extensive stress-induced reprogramming at 33°C, including widespread activation of oxidative phosphorylation, arginine/proline metabolism, and HSPs involved in cellular stress responses. This suggests that Carmel RKNs mitigate thermal stress through large-scale transcriptional adjustments, rather than innate heat tolerance. • The JV population exhibits an intermediate adaptive strategy, balancing DNA repair, autophagy, and protein stability to manage temperature fluctuations. This generalist response enables JV RKNs to maintain reproductive efficiency across varying thermal conditions. 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.