Results
Our results showed a clear shift in root morphology over time in seed
plants, with thinner root systems present in more derived lineages,
whereas Gymnosperms and Magnoliids showed thicker roots and lower SRL
values. RTD was relatively similar across groups (Fig 1), although it
decreased from woody to non-woody plants across phylogenetic groups (Fig
S1). The transition to ECM state had different effects on root
morphology depending on the phylogenetic group (Table 1, Figure S1).
Gymnosperms showed a substantial decrease in root diameter after
mycorrhizal change (Table S2) but this result is strongly dependent on
the sole divergence between the AM Cupressales and the ECM Pinales, so
the association between root diameter and mycorrhizal state was not
significant after phylogenetic correction (Fig. 2, Table 1). There was
evidence of an increase in RTD from AM to ECM species, but only for the
analysis on seed plants as a whole. On the other hand, there was no
evidence that the transition to associations with Dikarya fungi was
associated with root morphology in Rosids, suggesting that this group
already had thin roots, high SRL and relatively high RTD by the time
they acquired ECM capabilities. (Table 1, Fig 2). The loss of the
mycorrhizal symbiosis was significantly associated with root morphology
at the level of the seed plants and within some seed plant clades (Table
1). There were significant decreases in root diameter after switching to
NM state but mostly when comparing all plants (Table 1, Table S2, Figure
S1). SRL increased significantly for non-mycorrhizal groups when
compared to basal groups (Table 1) and within Asterids. Non-mycorrhizal
species also showed a decrease in RTD at the seed plant level and within
Monocots and Asterids. Finally, mycorrhizal changes were not associated
with leaf vein density, which corresponds with previous studies
reporting similar leaf traits among mycorrhizal groups (Koele et
al. 2012, Table S3)
We found a significant negative correlation of vein density with both
diameter and RTD but a positive relationship with SRL among current
species (Fig. 3). Moreover, leaf vein density mycorrhizal state and
growth habits were still significant once they were included in the
model (Table S4) but the significance of the association was lost after
phylogenetic corrections (Table 2), suggesting that the trend is
strongly influenced by the morphological difference between plant
clades. Habit was the only significantly associated factor with root
morphology within clades, suggesting that there are important changes in
root morphology associated with ecological strategies and lifespan. In
support of the “integrated” scenario, we found no significant effect
of mycorrhizal state in root traits after correction for habit and vein
density. The same result was obtained after removing Ericoid mycorrhizal
plants (data not shown), and after removing ECM species and testing only
for the transition from AM to NM (F = 0.13, p =0.8, F = 0.15, p =0.86
and F=0.97, p=0.38 for Diameter, SRL and RTD respectively). On the other
hand, habit remained highly significant (F = 22.9, p <0.0001,
F = 10.56, p <0.0001 and F=6.33, p=0.003, for diameter SRL and
RTD respectively). This suggests that the transition to herbaceous habit
seems to have meaningful effect on root morphology in Angiosperms (Table
2).
Finally, the ancestral reconstructions illustrate a shift in leaf
venation along with increases in SRL and thinner roots but not with RTD
trends (Fig 4). The reconstruction suggests that the ancestral seed
plants possessed relatively low SRL, intermediate root diameter and RTD,
in addition to low vein density. Root diameter in the Magnoliids, some
Eudicots and Monocots increased during time, suggesting that the coarse
distal roots represent a specialization rather than the ancestral stage.
During the diversification of Angiosperms in the mid-Creteaceous
emergent groups of Asterids and Rosids showed a substantial increase in
SRL, and reduction in root diameter as vein densities increased,
supporting the idea of a coordinated lift in plant hydraulics. In
addition, we detected a previously unreported evolutionary divergence in
RTD between Rosids and Asterids, with the former evolving to higher
values than other plant groups, whereas Asterids showed similar RTD
trends to those in the Monocots and Magnoliids clades.