How does genome size affect the evolution of pollen tube growth rate, a haploid performance trait?

PREMISE: Male gametophytes of most seed plants deliver sperm to eggs via a pollen tube. Pollen tube growth rates (PTGRs) of angiosperms are exceptionally rapid, a pattern attributed to more effective haploid selection under stronger pollen competition. Paradoxically, whole genome duplication (WGD) has been common in angiosperms but rare in gymnosperms. Pollen tube polyploidy should initially accelerate PTGR because increased heterozygosity and gene dosage should increase metabolic rates. However, polyploidy should also independently increase tube cell size, causing more work which should decelerate growth. We asked how genome size changes have affected the evolution of seed plant PTGRs. METHODS: We assembled a phylogenetic tree of 451 species with known PTGRs. We then used comparative phylogenetic methods to detect effects of neo-polyploidy (within-genus origins), DNA content, and WGD history on PTGR, and correlated evolution of PTGR and DNA content. RESULTS: Gymnosperms had significantly higher DNA content and slower PTGR optima than angiosperms, and their PTGR and DNA content were negatively correlated. For angiosperms, 89% of model weight favored Ornstein-Uhlenbeck models with a faster PTGR optimum for neo-polyploids, whereas PTGR and DNA content were not correlated. For within-genus and intraspecific-cytotype pairs, PTGRs of neo-polyploids < paleo-polyploids. CONCLUSIONS: Genome size increases should negatively affect PTGR when genetic consequences of WGDs are minimized, as found in intra-specific autopolyploids (low heterosis) and gymnosperms (few WGDs). But in angiosperms, the higher PTGR optimum of neo-polyploids and non-negative PTGR-DNA content correlation suggest that recurrent WGDs have caused substantial PTGR evolution in a non-haploid state.

Evolution of development of pollen performance.

With the origin of pollination in ancient seed plants, the male gametophyte ("pollen") began to evolve a new and unique life history stage, the progamic phase, a post-pollination period in which pollen sexual maturation occurs in interaction with sporophyte-derived tissues. Pollen performance traits mediate the timing of the fertilization process, often in competition with other pollen, via the speed of pollen germination, sperm development, and pollen tube growth. Studies of pollen development rarely address the issue of performance or its evolution, which involves linking variation in developmental rates to relative fitness within populations or to adaptations on a macroevolutionary scale. Modifications to the pollen tube pathway and changes in the intensity of pollen competition affect the direction and strength of selection on pollen performance. Hence, pollen developmental evolution is always contextual-it involves both the population biology of pollen reaching stigmas and the co-evolution of sporophytic traits, such as the pollen tube pathway and mating system. For most species, performance evolution generally reflects a wandering history of periods of directional selection and relaxed selection, channeled by developmental limitations, a pattern that favors the accumulation of diversity and redundancy in developmental mechanisms and the genetic machinery. Developmental biologists are focused on finding universal mechanisms that underlie pollen function, and these are largely mechanisms that have evolved through their effects on performance. Here, we suggest ways in which studies of pollen performance or function could progress by cross-fertilization between the "evo" and "devo" fields.

Morphological Plant Modeling: Unleashing Geometric and Topological Potential within the Plant Sciences.

The geometries and topologies of leaves, flowers, roots, shoots, and their arrangements have fascinated plant biologists and mathematicians alike. As such, plant morphology is inherently mathematical in that it describes plant form and architecture with geometrical and topological techniques. Gaining an understanding of how to modify plant morphology, through molecular biology and breeding, aided by a mathematical perspective, is critical to improving agriculture, and the monitoring of ecosystems is vital to modeling a future with fewer natural resources. In this white paper, we begin with an overview in quantifying the form of plants and mathematical models of patterning in plants. We then explore the fundamental challenges that remain unanswered concerning plant morphology, from the barriers preventing the prediction of phenotype from genotype to modeling the movement of leaves in air streams. We end with a discussion concerning the education of plant morphology synthesizing biological and mathematical approaches and ways to facilitate research advances through outreach, cross-disciplinary training, and open science. Unleashing the potential of geometric and topological approaches in the plant sciences promises to transform our understanding of both plants and mathematics.