Incorporating belowground traits: avenues towards a whole‐tree perspective on performance

Abstract

Tree performance depends on the coordinated functioning of interdependent leaves, stems and (mycorrhizal) roots. Integrating plant organs and their traits, therefore, provides a more complete understanding of tree performance than studying organs in isolation. Until recently, our limited understanding of root traits impeded such a whole‐tree perspective on performance, but recent developments in root ecology provide new impetuses for integrating the below‐ and aboveground. Here, we identify two key avenues to further develop a whole‐tree perspective on performance and highlight the conceptual and practical challenges and opportunities involved in including the belowground. First, traits of individual roots need to be scaled up to the root system as a whole to determine belowground functioning, e.g. total soil water and nutrient uptake, and hence performance. Second, above‐ and belowground plant organs need to be mechanistically connected to account for how they functionally interact and to investigate their combined impacts on tree performance. We further identify mycorrhizal symbiosis as the next frontier and emphasize several courses of actions to incorporate these symbionts in whole‐tree frameworks. By scaling up and mechanistically integrating (mycorrhizal) roots as argued here, the belowground can be better represented in whole‐tree conceptual and mechanistic models; ultimately, this will improve our estimates of not only the functioning and performance of individual trees, but also the processes and responses to environmental change of the communities and ecosystems they are part of.

Novel leaf-root coordination driven by leaf water storage tissues in mangroves

“…This is partially consistent with our second hypothesis for mangrove plants. Generally, under drought or physiological drought caused by high salinity, plant roots and vessels tend to be thinner 11,21,41,42,43 , whereas leaf water storage tissues usually increases 34,35,39 . These contrasting trends will cause a negative relationship between root diameter (representative of root hydraulics) and leaf water storage tissues (representative of leaf economics) in mangrove plants, which was confirmed by our results (Fig.…”

“…One conspicuous characteristic of mangrove plants is that they usually have significant water storage tissues in their leaves as an adaption to the imperative water demanding of transpiration under drought stress 12,13,14,15,16 . Meanwhile, plants usually adjust above- and belowground organs (e.g., leaves vs. roots) in a coordinated manner during plant evolution and response to changing environments 4,17,18,19,20,21 . However, little is known about how leaves, especially leaf water storage tissues , and roots vary across mangrove species and how above- and belowground coordination, if present, differs from that of non-mangrove plants.…”

Future for trees and forests

“…Yet, we do not yet fully understand such responses for large, structurally more complex, trees and we require better tree models for predicting their responses to climate variation. In addition we are just starting with integrating root and soil responses in such models (Weemstra et al 2020, Weemstra et al 2022), and we require upscaling of these tree responses to entire forests. These challenges receive major attention in my current and future research.…”

Linking rhizosphere soil microbial activity and plant resource acquisition strategy

“…Despite such intimate connections between plants and microorganisms in the rhizosphere, and considerable influences of plant species identity on rhizosphere processes have been identified (Cheng et al, 2014; Lambers et al, 2009; Lau & Lennon, 2011), the knowledge about how plant traits and associated resource acquisition strategies influence rhizosphere soil microbial activity needs further exploration. Typically, in previous reports, (i) most of our understanding on this topic centers around the connection of plant above‐ground traits and soil properties (De Vries et al, 2012; Garnier et al, 2004); (ii) roots and leaves are rarely considered as a unified whole, despite the fact that plant as a whole influences soils rather than through isolated organs (Weemstra et al, 2022) and (iii) the linkage of plant traits and soils is in the context of a one‐dimensional resource economics spectrum, neglecting the multivariate nature of plant below‐ground resource acquisition (i.e. multidimensional trait space) (Han et al, 2020; Henneron et al, 2020).…”

“…Typically, in previous reports, (i) most of our understanding on this topic centers around the connection of plant above-ground traits and soil properties (De Vries et al, 2012;Garnier et al, 2004); (ii) roots and leaves are rarely considered as a unified whole, despite the fact that plant as a whole influences soils rather than through isolated organs (Weemstra et al, 2022) and (iii) the linkage of plant traits and soils is in the context of a one-dimensional resource economics spectrum, neglecting the multivariate nature of plant belowground resource acquisition (i.e. multidimensional trait space) (Han et al, 2020;Henneron et al, 2020).…”