The Genetic Basis of Plant Functional Traits and the Evolution of Plant-Environment Interactions

Abstract

Leaves are the most conspicuous organs of plants and their form and function are key determinants of plant ecology. Moreover, energy captured by leaves through photosynthetic carbon reduction forms the base of nearly every terrestrial ecosystem. As such, the morphology and physiology of leaves have been a central focus of research on plant ecophysiology, development, and evolution. We review recent research on the genetic basis of leaf structure and nutrient profile, as well as stomatal patterning as exemplar traits for understanding the evolution of plant functional traits. We discuss available and emerging methods for determining the genetic basis of plant traits and then present a synthetic assessment of the molecular basis of each trait and the extent to which patterns of natural diversity are relevant to eco-evolutionary analysis. Overall, we find that research on the three traits has emerged from different sub-disciplines in biology. We have a deep understanding of the developmental genetics of leaf size and stomatal patterning and, to a lesser degree, leaf shape, though research on these has been limited to a small number of plant species. By contrast, there is a deep literature describing natural genetic diversity of leaf nitrogen content due, in part, to the ease of measuring this trait in large genetic mapping populations. The molecular control of leaf P concentration, on the other hand, has been severely understudied. For all three traits, there are few examples of studies that have empirically linked molecular genetic variation in specific genes with phenotypic diversity observed in natural populations of plants. We conclude by discussing present challenges with synthesizing different traditions in genetics, physiology, development and evolution and prospects for progress in the coming years. Table 1-Genes involved in the control of leaf size through regulation of the initiation, cell division, and transition phases, with mechanisms and relevant references. Symbol Gene name Control of leaf size Reference(s) CKX1-6 CYTOKININ OXIDASE/DEHYDROGENASE 1-6 Overexpression leads to a decrease in number and size of meristematic cells, as well as a decrease in leaf expansion rate/duration Werner et al. (2001; 2003) Holst et al. (2011) Brenner (2012) CKS1 CYCLIN-DEPENDENT KINASE SUBUNIT 1 Overexpression causes inhibition of cell-cycle progression, leading to reduced meristem size De Veylder et al. (2001) SWP STRUWWELPETER struwwelpeter mutants shows a shorter window of cell-proliferation at the leaf primordium stage Autran et al. (2002) Clay & Nelson (2005) REV1 REVOLUTA rev-1 mutants cannot properly limit cell divisions at the leaf meristem, which leads to larger leaves Talbert et al. (1995) APC10 ANAPHASE PROMOTING COMPLEX 10 Overexpression leads to increased cell division rates at the early stages of leaf development Capron et al. (2003) Eloy et al. (2011) CDC27a CELL DIVISION CYCLE PROTEIN 27 HOMOLOG A Overexpression leads to increased cell-division rates during the entire life cycle of the plant Rojas et al....

Quantitative trait locus mapping reveals an independent genetic basis for joint divergence in leaf function, life-history, and floral traits between scarlet monkeyflower (Mimulus cardinalis) populations

“…If so, trait syndromes evolve via alleles with pleiotropic effects on multiple traits (Troth et al, 2018;Martínez-Berdeja et al, 2020), establishing strong genetic correlations that may constrain or accelerate adaptation to novel environmental conditions depending on the direction of multivariate selection. Alternatively, convergent integration of traits across gradients may reflect independent local adaptation to shared environmental factors in the absence of any necessary functional connection (reviewed in Donovan et al, 2011;Agrawal, 2020;Guilherme Pereira and Marais, 2020). In the latter case, trait correlations can be readily broken up by gene flow and recombination, allowing relatively unconstrained adaptation along individual trait axes in response to novel selection pressures.…”

Quantitative trait locus mapping reveals an independent genetic basis for joint divergence in leaf function, life‐history, and floral traits between scarlet monkeyflower (Mimulus cardinalis) populations

“…If so, trait syndromes evolve via alleles with pleiotropic effects on multiple traits (Troth et al, 2018; Martínez‐Berdeja et al, 2020), establishing strong genetic correlations that may constrain or accelerate adaptation to novel environmental conditions depending on the direction of multivariate selection. Alternatively, convergent integration of traits across gradients may reflect independent local adaptation by individual traits to shared environmental factors in the absence of any necessary functional connection (reviewed in Donovan et al, 2011; Agrawal, 2020; Guilherme Pereira and Marais, 2020). These different genetic bases for trait associations within species imply that distinct processes could underlie current patterns of diversity and also make divergent predictions about evolutionary responses to environmental change.…”

“…It is tempting to conclude that such cross‐population associations, as well as larger scale patterns, arise from genetic correlations caused by pleiotropy (multiple effects of single genes) or tight linkage (Lowry and Willis, 2010). However, despite abundant heritable variation in leaf functional traits within species (Ackerly et al, 2000; Geber and Griffen, 2003; Guilherme Pereira and Marais, 2020), there is little evidence of genetic coordination among them (Muir and Moyle, 2009; Muir et al, 2014; Taylor et al, 2016; Coneva et al, 2017; Coneva and Chitwood, 2018). Evidence of genetic coordination of physiology or leaf structure with fast‐slow traits at the whole‐plant level has been even more elusive (Ivey et al, 2016).…”

“…Evidence of genetic coordination of physiology or leaf structure with fast‐slow traits at the whole‐plant level has been even more elusive (Ivey et al, 2016). However, the genetics of both leaf functional traits and life history variation remain poorly understood outside a few model systems (reviewed in Guilherme Pereira and Marais, 2020), and further investigation of the joint genetic architecture of leaf‐scale and whole‐organism traits within species is needed.…”