Inflorescence preformation prior to winter: a surprisingly widespread strategy that drives phenology of temperate perennial herbs

Abstract

Organ preformation in overwintering buds of perennial plants has been known for almost two centuries. It is hypothesized to underlie fast growth and early flowering, but its frequency, phylogenetic distribution, and ecological relevance have never been systematically examined. We microscopically observed inflorescence preformation in overwintering buds (IPB) in the autumn. We studied a phylogenetically and ecologically representative set of 330 species of temperate perennial angiosperms and linked these observations with quantitative data on species' flowering phenology, genome size, and ecology. IPB was observed in 34% of species examined (in 14% species the stamens and/or pistils were already developed). IPB is fairly phylogenetically conserved and frequent in many genera (Alchemilla, Carex, Euphorbia, Geranium, Primula, Pulmonaria) or families (Ranunculaceae, Euphorbiaceae, Violaceae, Boraginaceae). It was found in species of any genome size, although it was almost universal in those with large genomes. Compared with non-IPB species, IPB species flowered 38 d earlier on average and were more common in shaded and undisturbed habitats. IPB is a surprisingly widespread adaptation for early growth in predictable (undisturbed) conditions. It contributes to temporal niche differentiation and has important consequences for understanding plant phenology, genome size evolution, and phylogenetic structure of plant communities.

Winter belowground: Changing winters and the perennating organs of herbaceous plants

“…Species with preformed inflorescences within overwintering buds generally flower early and are common in habitats with high shade and low disturbance, or in habitats with a short growing season (e.g. arctic, alpine, and forest geophyte communities) (Meloche & Diggle, 2001;Schnablová et al, 2021). Bud preformation is phylogenetically conserved in many genera and families (Schnablová et al, 2021).…”

“…arctic, alpine, and forest geophyte communities) (Meloche & Diggle, 2001;Schnablová et al, 2021). Bud preformation is phylogenetically conserved in many genera and families (Schnablová et al, 2021). Despite the advantage of rapid spring growth for plants with preformed buds, these species have limited flexibility to respond to changes in environmental conditions (Diggle, 1997;Werger & Huber, 2006).…”

“…Specifically, they emerge aboveground later than plants growing from shallowly positioned organs, and they must invest more of their storage carbohydrates to grow upwards through the soil (Klimeš, Klimešová, & Osbornová, 1993). However, many geophyte ephemeral species preform structures within buds so that spring growth to reach the soil surface primarily involves taking up additional water to inflate the cells, which helps overcome the cost of delayed emergence (Schnablová et al, 2021).…”

The growing and vital role of botanical gardens in climate change research

“…first leaf out, which can be difficult) of herbaceous plants in botanical gardens (Nordt et al ., 2021). The Botanical Garden at Charles University in Prague has shown the way forward in this field, demonstrating that differences among herbaceous species in light levels and mature plant heights influence plant growth phenology (Huang et al ., 2018; Schnablová et al ., 2020).…”

Preforming floral primordia converge on a narrow range of stages at dormancy despite multiple effects of temperature on development

“…The expansion of a mature flower at anthesis, however, is just one stage of what can be a lengthy developmental process. In most taxa of temperate and higher latitude environments, floral primordia are initiated a year or more in advance of maturation, a process known as preformation (Diggle, 1997; Klimešová et al ., 2017; Schnablová et al ., 2021). Little is known about development in preforming species, and the effects of environmental conditions on development over the year(s)‐long period of flower preformation have rarely been examined (reviewed in Diggle & Mulder, 2019).…”