The mutualistic relationship between mycorrhizae fungi and plant roots is crucial for plant establishment in almost all terrestrial ecosystems. However, how this symbiosis influences plant ecological strategies, particularly the trade-off between resource allocation for growth and survival, remains poorly understood (McCormack and Iversen, 2019; Freschet et al., 2021b). Research into general patterns of root resource acquisition has revealed that co-variation among root traits parallels co-variation among analogous leaf traits, leading to the concept of a one-dimensional axis of variation known as the ‘root economic spectrum’ (Withington et al., 2006; McCormack et al., 2012; Reich, 2014). On one end of this spectrum, traits favor rapid resource uptake and growth (e.g., roots with high nitrogen content [RNC] and specific root length [SRL]); at the other end, traits promote longevity and slower growth (e.g., roots with large diameters [RD] and high tissue density [RTD]) (Weemstra et al., 2016; Roumet et al., 2016). However, recent findings suggest that root traits may vary along two dimensions (Kong et al., 2014; Kramer-Walter et al., 2016), which may be partly explained by their association with arbuscular mycorrhizae (AM). A recent hypothesis highlights the critical role of AM in explaining the multidimensional nature of root resource acquisition strategies (Bergmann et al., 2020). The relationship between AM and roots provides alternative pathways of resource uptake, allowing plants to adapt to changes in resource availability (Ma et al., 2018; McCormack and Iversen, 2019; Bergmann et al., 2020). Understanding the relationship between roots and AM is thus crucial to unraveling the complex variation in root traits and their influence on plant ecological strategies.

Roots exhibit significant phenotypic variation, enabling efficient uptake of water and nutrients (Kenrick and Crane, 1997; Kramer-Walter et al., 2016; Iversen et al., 2017), which is crucial for plant performance in resource-limited environments. However, root traits alone do not always fully capture a plant’s functional root strategy. For most plants (ca. 80%), resource acquisition relies on a partnership with mycorrhizal fungi (Smith and Read, 2008; Brundrett, 2009), particularly with AM. Recognizing the role of AM and incorporating them into analyses of root trait co-variation has deepened our understanding of the phenotypic multidimensionality of root traits (McCormack and Iversen, 2019). This approach has led to identifying two primary axes of trait co-variation, referred to as the ‘Root Economics Space’ (RES) (Bergmann et al., 2020). The first axis relates to resource acquisition strategies and is determined by the co-variation between SRL and RD (Ma et al., 2018; Bergmann et al., 2020), which is strongly influenced by the association with AM. Specifically, greater AM colonization is associated with species with larger RD (Comas et al., 2014; Valverde-Barrantes et al., 2017). Along this ‘collaboration gradient,’ species with fine, low-cost roots (e.g., high SRL and low RTD) can explore and obtain soil resources independently (a ‘do it yourself’ strategy) (Bergmann et al., 2020), while species with thicker roots can adopt an “outsourcing” strategy, relying on mycorrhiza for resource acquisition (Bergmann et al., 2020). The second axis aligns with the fast-slow plant economics spectrum (Reich, 2014). It is determined by the co-variation between RNC and RTD, which reflect metabolic rates and tissue conservation (Eissenstat et al., 2015).

The RES has been demonstrated across species from various biomes, but arid ecosystems remain significantly underrepresented, with data available for only a few species (n=10), accounting for less than 2% of the total species sampled (Bergmann et al., 2020). In these environments, AM are particularly important for plant performance, enhancing resistance to water and nutrient scarcity (Khudairi, 1969; Allen, 2007; Qiao et al., 2019). AM also mediate tolerance to other abiotic stressors in deserts, such as heat and salinity (Rodriguez et al., 2008; Madouh and Quoreshi, 2023), and may play a critical role in survival through protection mechanisms (Freschet et al., 2021b). Notably, mycorrhizal colonization tends to increase with environmental stress (Allen et al., 2003; Kivlin et al., 2013; Aguilera et al., 2016), suggesting that the intensity and integration of AM colonization with root traits could indicate the relevance of mycorrhizal associations in shaping resource acquisition strategies and survival in extreme environments (Freschet et al., 2021b).

To better understand the ecological significance of root strategies, the relationship between root traits and AM colonization can be modeled as a phenotypic network (He et al., 2020). In this network, nodes represent root traits, and edges indicate strong correlations between them. This framework helps identify the most central or interconnected traits (i.e., ‘hub-traits’) and their influence on root strategies (Kleyer et al., 2019; Rao et al., 2023). If AM colonization strongly correlates with multiple root traits and spans more than one dimension of trait co-variation, it likely plays a multifaceted role in root strategies, leading to high network connectivity mediated by AM. Despite the potential insights from this network approach, few studies have explored root trait relationships in this way (see Kleyer et al., 2019; Rao et al., 2023; Ye et al., 2024). Incorporating AM colonization into network analysis could reveal its role in shaping root strategies, particularly in extreme desert environments.

Deserts pose significant challenges to many life forms due to their highly variable environmental conditions. In these environments, high aridity can reduce the diversity and abundance of mycorrhizas (Berdugo et al., 2020; Weber et al., 2019), potentially affecting their symbiotic relationship with plants (Millar and Bennett, 2016). Furthermore, as aridity increases, variation of root traits linked to resource acquisition, such as RNC, tends to increase beyond a certain threshold. This suggests that in extremely arid conditions, plants might benefit from adopting strategies that enable rapid resource uptake during brief periods of availability (Carvajal et al., 2019; de la Riva et al., 2021). While plants in arid environments display a range of root strategies to thrive in these challenging conditions, it remains unclear whether these include a ‘collaboration axis’ with mycorrhizal fungi. Expanding predictions of the RES (sensu Bergmann et al., 2020) to encompass a broader range of conditions requires studies that consider root trait variation alongside quantitative data on AM in arid ecosystems.

The Coastal Atacama Desert (CAD) in Chile, recognized as the world’s driest desert, is a hyper-arid environment along most of its extent. In this environment, where prolonged droughts can lead to the complete loss of aboveground plant organs, long-lived woody shrubs thrive despite severe water scarcity. Previous studies have shown that these shrubs possess diverse root systems with high and variable root trait covariation along water and nutrient gradients (Squeo et al., 1999; Morales et al., 2014). However, this variation does not always align with the predictions of the RES (Carvajal et al., 2019; Delpiano et al., 2020). The functional role of AM in the CAD remains largely unexplored. Despite this, AM colonization has been documented even in the driest regions of this ecosystem and across various plant families, including those traditionally considered non-mycorrhizal (Dhillion et al., 1995; Aguilera et al., 1998). Although direct evidence linking root functional traits to AM colonization is lacking, it is expected that AM to play a key role in determining the survival and growth strategies of plants in this extreme environment.

In this study, we explore below-ground ecological strategies under the extreme aridity conditions of the CAD. We sampled absorptive fine roots from 32 dominant shrub species to examine root trait co-variation and their relationship with mycorrhizal fungi. We hypothesized that variation in fine root traits at the species level is linked to mycorrhizal colonization, supporting the existence of a ‘collaboration gradient’. We predicted that an increase in fine root diameter in shrubs would correlate with increased mycorrhizal colonization. Additionally, mycorrhizae colonization would be highly interconnected and central in the root trait network (i.e., a hub-node), underscoring the vital role of mycorrhizal associations in shaping root ecological strategies in arid environments.

Our study explored the intricate relationship between root traits and arbuscular mycorrhizal (AM) colonization in shrub species, revealing valuable insights into plant adaptation strategies in extremely arid ecosystems. Despite substantial variation in root trait attributes and the inclusion from species studied of different orders, including Caryophyllales, we consistently observed AM colonization. Notably, species with larger root diameters tended to exhibit higher levels of AM colonization, supporting the existence of an ‘outsourcing’ strategy along| the ‘collaboration gradient’. Furthermore, the significant correlations between AM colonization and other root traits highlight the complexity of the root phenotypic network, where AM colonization plays a central role in establishing connections among traits. These findings emphasize the importance of AM colonization in shaping root ecological strategies for shrub species in extreme arid ecosystems.

The results revealing that species with greater RD tend to have higher colonization rates support our hypothesis that fine root trait variation at the species level is linked with mycorrhizal fungi colonization, consistent with the ‘collaboration gradient’ (Bergmann et al., 2020). These findings suggest that thicker roots have a higher potential for colonization, likely because they provide more internal space for AM fungi. As RD increases, the cortex area expands faster than the stele, offering more habitat for fungi (Kong et al., 2019; Zhang et al., 2024). The negative relationship between RD and RTD further supports this, as parenchymatous cortical tissue is less dense than stele tissue (Valverde-Barrantes et al., 2016). A higher colM may enhance nutrient absorption in thicker roots, as AM are well-adapted to acquire N, P, and water from the soil (McCormack and Iversen, 2019; Freschet et al., 2021a). The phylogenetic conservatism observed in RD and RTD ( Supplementary Table S3 , Supplementary Material ) suggests that this trait combination reflects an early-derived ecological strategy that enhances nutrient-foraging (mainly P) by maximizing cortex area available for AM colonization (Chen et al., 2013; Kong et al., 2017). In addition, our results show that colM and SRL are unrelated, contrasting the expected pattern of the ‘collaboration gradient’ expected in the RES. This may be explained by the fact that all species in our study have high RD values (> 0.4 mm, Supplementary Table S2 , Supplementary Material ), where sufficient cortex space exists for AM colonization regardless of SRL (Kong et al., 2014).

Although our results highlight the multidimensional nature of root traits, their patterns of covariation partially deviate from the expectations of the global RES. Specifically, our analysis shows that the second axis of the pPCA primarily captures the covariation between RNC and RC:N rather than with RTD. Interestingly, RD and colM are also associated with this second axis. Thus, species with higher RNC, lower RC:N, and thinner roots align with the ‘fast’ end of the spectrum, while species with lower RNC, high RC:N, and thicker roots occupy the ‘slow’ end. Fine root lifespan increases with RC:N and decreases with rising RNC (Hou et al., 2024), suggesting that the positive relationship between RC:N with root lifespan may attributed to higher concentrations of recalcitrant compounds, such as lignin and suberin, which enhance root resistance to herbivores and pathogens in the soil (Wardle et al., 2004).

Several studies have found a negative relationship between RNC and root lifespan (Withington et al., 2006; Reich, 2014; Hou et al., 2024), as RNC is often positively associated with higher metabolic activity and respiration rates (Reich et al., 2008; Roumet et al., 2016). However, RNC also plays other functional roles, such as facilitating nutrient uptake, enzyme activity, and N storage (Reich et al., 2008; Liu et al., 2015; Freschet et al., 2021a). In our study, RNC did not exhibit a significant phylogenetic signal ( Supplementary Table S3 , Supplementary Material ), suggesting that its variation across species is likely shaped by environmental factors, such as soil fertility (Craine et al., 2005; Holdaway et al., 2011). Accordingly, a study of shrub communities in the southern CAD found a positive relationship between RNC and N soil availability (Delpiano et al., 2020), indicating that RNC is primarily influenced mainly by soil N availability in nutrient-limited environments (Zangaro et al., 2008; Zhang et al., 2018; Chapin et al., 1993). Although direct evidence linking RNC to root lifespan is limited, our findings suggest a complex interplay between RNC, environmental conditions, and root functional traits in arid ecosystems.

Several studies have consistently shown that RD plays a more significant role than RTD in determining root lifespan (McCormack et al., 2012; Ma et al., 2018; Kong et al., 2019; Hou et al., 2024), a finding that aligns with our results. McCormack et al. (2012) suggest that this relationship reflects a resource optimization strategy, where the increase in root lifespan with greater RD ensures better nutrient and water returns by investing more carbon in thicker roots than thinner ones. Additionally, higher colM in thicker roots may contribute to increased root lifespan due to the fungi’s role in plant defense against pathogens by producing secondary metabolites (Hou et al., 2024). Increased colM can also reduce root turnover rates, maximizing root foraging activity by expanding surface area (Aguilera et al., 2016; Shen et al., 2023) and enhancing resource availability (Augé, 2001; Allen, 2007; Qiao et al., 2019).

The phenotypic network analysis revealed that colM acts as a hub trait, highlighting its central role in structuring the root phenotypic network (He et al., 2020). In the hyper-arid CAD, colM mediates more functional trade-offs within the root phenotype than would be expected by chance (Bergmann et al., 2020). When colM is excluded from the network, traits such as RD, RTD, and RDMC become more prominent, but overall network connectivity declines. This underscores the role of colM in maintaining the interconnectedness of the root phenotypic network (Ye et al., 2024). These findings suggest that colM contributes to multiple root functions and shapes root ecological strategies (Freschet et al., 2021a).

The environmental conditions of the CAD impose several constraints on the survival of nearly all organisms (Maestre et al., 2015; Berdugo et al., 2020). Hyperaridity significantly limits water availability and slows biogeochemical cycles, resulting in low availability of soil nutrients like N, P, and K (Noy-Meir, 1973; Schlesinger et al., 1996). Given that shrubs in this region are long-lived, every individual will likely endure at least one period of intense drought during its lifespan (Carvajal et al., 2019). As a result, species must develop belowground strategies that extend root lifespan and optimize resource uptake when nutrients and water become available. In this context, having thick roots combined with high levels of colM seems to be the optimal functional strategy for shrubs to thrive under the extreme, hyper-arid conditions of the CAD.

Our results offer new insights into plant adaptations in extreme arid ecosystems by linking root traits and arbuscular mycorrhizal colonization in 32 shrub species. We found that root trait covariation is multi-dimensional, with RD and colM playing key roles in shaping both dimensions of root ecological strategies. This finding differs from the global RES but aligns with recent studies linking RD and colM to the fast-slow ecological spectrum. To enhance our understanding of global root strategies, it is crucial to incorporate more quantitative data on root traits and AM colonization from underrepresented biomes. Network theory also proves to be a valuable complement PCA, effectively unraveling the complex, multidimensional relationships among root traits and their ecological roles. Given the significant role of AM in extreme environments, further research is needed to elucidate the mechanisms by which AM shapes root ecological strategies. In this context, the Coastal Atacama Desert provides an ideal natural laboratory for studying the effects of aridity on terrestrial ecosystems.