Evolution of root morphology and leaf vein density during the
diversification of Angiosperms
Our study shows for the first time that root systems could have been
subjected to strong selection and rapid modification during the
diversification of Angiosperms during the Late Cretaceous. To date, the
role of fine roots has not been fully included in the discussion about
the diversification and expansion of flowering plants. The increases in
vein density during Angiosperm radiation have been linked to increased
gas exchange and thus higher photosynthetic rates, which could have been
favored when climate became colder, drier and growing season length
decreased in temperate regions (Franks & Beerling 2009). Higher vein
densities and associated increases in hydraulic conductance also allow
plants to maintain open stomata under drier soil conditions (Brodribb &
Holbrook 2004). However, increases in leaf evaporation due to higher
stomatal conductance (Hetherington & Woodward 2003; Boyce & Lee 2010)
requires more efficient conductance in vessel anatomy (Christman &
Sperry 2010, Feild & Brodribb 2013) and xylem traits (Morris et
al. 2016, Nardini & Jansen 2013). Our findings suggest that higher
SRL, smaller diameters, and higher tissue density modifications in the
Rosids was coordinated with other modifications to achieve more
efficient photosynthesis and may help to explain the dominance of Rosids
as major components of forests globally (Wang et al. 2009). Other
groups adapted to colder and dried conditions by reducing their lifespan
and acquiring an herbaceous habit (Zanne et al. 2016). Asterids
and Monocots, both groups largely represented by herbs, increased SRL
but evolved lower RTD, possibly as an adaptation to limit root
investments in herbs with shorter lifespan.
We propose that the mechanism causing the decrease in root diameter and
increase in SRL was a reduction in root cortical tissue (Kong et
al. 2017). Physiological studies in fine roots have shown that
hydraulic resistance substantially increases with the thickness of
cortical tissue (Steudle &
Peterson1998,
Huang &
Eissenstat 2000);
and the production of thin, ephemeral roots is a coping mechanism for
periodic droughts (Chen et al. 2013). Decreases in diameter and
increases in SRL are also mechanisms associated with the increase in
root surface area in poor soils (Prieto et al. 2015). Moreover,
comparisons across angiosperm trees have shown that reductions in
cortical tissue were much more pronounced than stele diameter
(Valverde-Barrantes et al. 2016), suggesting a strong selection
for the reduction in cortex as the main contributor to the evolution of
finer roots, rather than an even decrease in all root tissues (Konget al. 2019). Then, increase the capacity to capture water and
move it efficiently into the vascular tissue to cope with higher
photosynthetic demands. In any case, the acceleration of belowground
metabolic activity during the diversification of Angiosperms may have
contributed largely to the increased weathering of parent material and
decreased atmospheric CO2 levels during Cretaceous
period (Raven and Edwards 2001, Pälike et al. 2012).
These patterns in root modifications indicate that the development of a
more efficient root system was an adaptation to cope with more unstable
and drastic climatic conditions, possibly enhanced by a later adoption
of ECM fungi in colder areas (Brundett and Tedersoo 2018).
Interestingly, the increase in diameter in the Magnoliids and other
families seem a derived condition from an ancestral intermediate value,
suggesting that the “magnoliid” type of root is a specialized
adaptation for nutrient foraging. Albeit the loss of the mycorrhizal
symbiosis was associated with finer roots in some clades, it is unlikely
that the two variables were causally related because of underlying
covariation with plant habit (i.e., finer roots in NM species may have
evolved because of herbaceousness). The hydraulic and metabolic shifts
experienced by flowering plants during angiosperm radiation in the Late
Cretaceous, resulting in the combination of highly efficient roots and
leaves, could have allowed Eudicots to become dominant in temperate and
boreal areas, whereas other Angiosperm groups with thicker root systems
were favored in warmer biomes (Wang et al. 2009, Chen et
al. 2013). Further studies in low latitude ecosystems are urgent in
order to understand the foraging activity of plants in these ecosystems,
and how they may change in future climatic scenarios.
Our analysis can also help to create more robust predictions about
future distributions of plant groups. Future increase in atmospheric
CO2 concentration, coupled with a warming climate, could
shift the geographic distribution of particular groups of plants. In the
past, climatic changes may have favored a subset of species that already
possessed fine roots that facilitate soil foraging when nutrients became
increasingly retained in inorganic matter in colder environments
(Ostonen et al. 2007). Future climate changes may benefit species
with thicker roots that could benefit to a greater extent from enhanced
mineralization rates under a warmer climate. Since changes in root
morphology seem highly conserved across phylogenies (Ma et al.2017), it is possible that arboreal groups in the Magnoliids and
Asterids, currently limited by climatic conditions, could start to
expand their natural ranges to higher latitudes and altitudes (Fadriqueet al. 2018). Future synthesis and modelling work will need to
integrate roots as an important component in global plant vegetation
models to better understand how plant communities may react to expected
climatic changes (Verheijen et al. 2013).