Evolution and ecology of plant architecture: integrating insights from the fossil record, extant morphology, developmental genetics and phylogenies

Background In contrast to most animals, plants have an indeterminate body plan, which allows them to add new body parts during their lifetime. A plant's realized modular construction is the result of exogenous constraints and endogenous processes. This review focuses on endogenous processes that shape plant architectures and their evolution. Scope The phylogenetic distribution of plant growth forms across the phylogeny implies that body architectures have originated and been lost repeatedly, being shaped by a limited set of genetic pathways. We (1) synthesize concepts of plant architecture, so far captured in 23 models; (2) extend them to the fossil record; (3) summarize what is known about their developmental genetics; (4) use a phylogenetic approach in several groups to infer how plant architecture has changed and by which intermediate steps; and (5) discuss which macroecological factors may constrain the geographic and ecological distribution of plant architectures. Conclusions Dichotomously branching Paleozoic plants already encompassed a considerable diversity of growth forms, here captured in 12 new architectural models. Plotting the frequency of branching types through time based on an analysis of 58 927 land plant fossils revealed a decrease in dichotomous branching throughout the Devonian and Carboniferous, mirrored by an increase in other branching types including axillary branching. We suggest that the evolution of seed plant megaphyllous leaves enabling axillary branching contributed to the demise of dichotomous architectures. The developmental-genetic bases for key architectural traits underlying sympodial vs. monopodial branching, rhythmic vs. continuous growth, and axillary branching and its localization are becoming well understood, while the molecular basis of dichotomous branching and plagiotropy remains elusive. Three phylogenetic case studies of architecture evolution in conifers, Aloe and monocaulous arborescent vascular plants reveal relationships between architectural models and show that some are labile in given groups, whereas others are widely conserved, apparently shaped by ecological factors, such as intercepted sunlight, temperature, humidity and seasonality.