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.