From shoot to leaf: step-wise shifts in meristem and KNOX1 activity correlate with the evolution of a unifoliate body plan in Gesneriaceae.

Abstract

Typical dicots possess equal-sized cotyledons and leaf-bearing shoots topped with a shoot apical meristem (SAM), the source of lateral organs, and where KNOX1 homeobox genes act as key regulators. New World Gesneriaceae show typical cotyledons, whereas Old World Gesneriaceae show anisocotyly, the unequal post-germination growth of cotyledons, and include unifoliate (one-leaf) plants. One-leaf plants show an extremely reduced body plan: the adult above-ground photosynthetic tissue consisting of a single cotyledon, a macrocotyledon enlarged by the basal meristem (BM), but lacking a SAM. To investigate the origin and evolution of the BM and one-leaf plants, the meristem activity and KNOX1 SHOOTMERISTEMLESS (STM) expression in cotyledons and leaves were systematically studied by RT-PCR and in situ hybridization across the family Gesneriaceae, Jovellana in Calceolariaceae (sister family to Gesneriaceae), and Antirrhinum in Plantaginaceae, all families of order Lamiales (asterids), in comparison to Arabidopsis (Brassicales, rosids). In all examined Lamiales samples, unlike Arabidopsis, BM activity accompanied by STM expression was found in both cotyledons in early stages. Foliage leaves of Gesneriaceae and Jovellana also showed the correlation of BM and STM expression. An extension of BM activity was found following a phylogenetic trajectory towards one-leaf plants where it is active throughout the lifetime of the macrocotyledon. Our results suggest that KNOX1 involvement in early cotyledon expansion originated early on in the diversification of Lamiales and is proposed as the prerequisite for the evolution of vegetative diversity in Gesneriaceae. Step-wise morphological shifts, driven by transfers of meristematic activity, as evidenced by shifts in KNOX1 expression, may be one mechanism by which morphological diversity evolves in plants.