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).