Evolution of mycorrhizal state and root morphology within seed plant clades
Our results contradict the expected close evolutionary relationship between root morphology and mycorrhizal association (Egerton-Warburton & Allen, 2001, Guo et al. 2008, Comas & Eissenstat 2009) and suggest that many of the traits previously associated to ECM associations (Brundrett & Tedersoo 2018) were actually achieved by most Angiosperms groups before departures from the ancestral AM stage. In fact, our results are consistent with more recent findings suggesting that switches to ECM association had limited effects on root morphology (Valverde-Barrantes et al. 2017), especially when closely related species are compared (Comas & Eissenstat 2009, Comas et al.2014, Kubish et al. 2016, Valverde-Barrantes et al. 2018).
Our study suggests that the association between root morphology and the loss of the mycorrhizal mutualism (the NM state) is complex. The presence of very fine root systems has been described in several non-mycorrhizal families such as Caryophyllaceae (Magallon & Castillo 2009), the carnivorous Droseraceae and Nepenthaceae (Adlassing et al. 2005), Proteaceae and Ranunculaceae (Brundrett 2017) as well as cluster roots in the Fagales (Lambers et al. 2008). However, our analyses revealed that the transition to NM state is confounded with habit, even after phylogenetic information was included in the analysis (Table 2, Table S2). Indeed, the herbaceous plants are known to have higher SRL, smaller root diameter and lower RTD than woody plants, which confers lower construction cost, faster turnover rates and faster nutrient acquisition compared to woody plants (McCormack et al.2012). As a result, NM plants likely report on average finer roots than other mycorrhizal groups because they are almost exclusively herbaceous. Moreover, the faster life history of the herbaceous habit, and their tendency to proliferate in disturbed habitats, could further limit associations with mycorrhizal fungi since plants in these environments are unlikely to obtain a net benefit from colonization by AM fungi (Peat & Fitter 1993). This does not mean that all herbaceous plants evolved independence from mycorrhizal associations. Root systems of important groups of herbs, including the entire order of Zingiberales, and Commelinales (Monocots) and several largely herbaceous families like Piperaceae (Magnoliids), Lamiaceae (Asterids) and Urticaceae (Rosids) have been poorly sampled so far but reported as associated largely with AM fungi (Wang & Qiu 2006). Future developments in these groups could change our perspective of the relationships between habit and mycorrhizal affiliations.
It is important to point out that these conclusions are based on the assumption of relatively fast transitions from one type of mycorrhizal association to others, and relatively few episodes of change between the ancestral AM stage and novel acquisition strategies. Although it has been stated that switches in mycorrhizal affiliations are rare because of the complex genetic signaling involved in the establishment and the stabilizing selection associated with the mycorrhizal mutualism (Delauxet al. 2014), intermediate stages can be important as transitional steps in the acquisition of a novel strategy for nutrient acquisition (Maherali et al. 2016). For instance, plant species engaging in mutualisms with multiple mycorrhizal types (e.g., AM and ECM) are frequently reported (Gehring et al. 2006). If these lineages represent an intermediate between mycorrhizal states, studying them in more detail could assist in unraveling the relationship between root evolution and mycorrhizal evolution, and is therefore a promising field for future research.
An important task to develop in future work is to acquire integrated data for entire plants, including root and leaf traits in the same individuals (Cordlandwehr et al. 2013, Medeiros et al.2017), rather than efforts to compile information from independent studies. Leaf and root traits can be affected substantially due to local conditions, and that intraspecific variability can only be accounted if traits are measured in an integrated fashion (Violle et al.2012). More importantly, this study detected an important information gap between root and leaf functional traits, particularly vein density, due to the historical focus on the venation pattern of broadleaf species (Boyce et al. 2009). Further studies in leaf venation patterns in groups with dominant parallel venation (i.e., Gymnosperms and Monocots) will help to elucidate how root and leaf traits evolved in these groups.
We also need more detailed reconstructions of the evolutionary pathway of root modifications over time for families with particularly diverse mycorrhizal strategies. For instance, families related to NM groups like Polygonaceae, Plumbaginaceae and Rhabdodendraceae (in Caryophyllales), Eupteleaceae (Ranunculales) or Sabiaceae (Protelaes) also contain either AM or ECM associations, but we know little about the morphology of those root systems to infer the role of root morphology on the departure from the AM state. Similarly, more detail studies within closely related groups could help to elucidate the relationship between root morphology and mycorrhizal associations (Brundrett 2017). For instance, recent studies in botanical gardens showed large variation in root diameters within the genus Rhododendron (Ericaceae, Medeiros et al.2017), a genus that is usually reported as forming ericoid associations (Wang & Qiu 2006) but can also associate with AM fungi (Chaurasiaet al. 2005). Unfortunately, no studies so far paired mycorrhizal and root morphology information in a phylogenetically controlled experiment. Future studies that match mycorrhizal associations with morphological syndromes among closely related species in common gardens can vastly improve our understanding of the evolution between root morphology, mycorrhizal associations and ecological strategies in seed plants.