How did the flower originate?

Abstract

The flower is a characteristic feature of angiosperms. The innovation and diversification of the flower significantly improve the reproductive efficiency and environmental adaptation of angiosperms, and thus contribute to the great success of angiosperms in terrestrial ecosystem. How the flower originated is a major aspect of Darwin’s “abominable mystery” of the origin and rapid diversification of angiosperms, and has long been a basic question of evolutionary biology and botany with intense investigations. Over the past two centuries, many theories and hypotheses have been proposed to explain the origin of the flower based on a broad spectrum of multidisciplinary research involving comparative morphology, paleontology, anatomy, and developmental biology. However, the answer to how the flower originated has remained controversial because the phylogeny of the seed plants was poorly resolved and the molecular basis of flower development was not unraveled. In 2005, Science posed this question as one of the 125 most challenging scientific questions in a special issue to commemorate the 125th anniversary of the journal, implying that the study of the process and mechanisms of the origin of the flower is still a hot topic of current evolutionary biology and botany. In recent years, thanks to the rise and rapid progress in molecular phylogenetics, evolutionary developmental biology (evo-devo), and genomics, new ideas have been brought and our knowledge on the origin of the flower has been updated. Now, it is generally believed that (i) the flower is a determinate, compressed, and bisexual reproductive axis, which consists of perianth, androecium, and gynoecium from the outer to the inner; (ii) the flower did not originate abruptly but evolved gradually, with bisexuality being the first step, followed by the compression of reproductive axis and the evolution of the floral determinacy, and the floral structural elements originated at different evolutionary stages; and (iii) the floral MADS-box genes that specify the identities of floral organs have experienced duplication events prior to the origin of the angiosperms and the changes in their expression patterns, functions, and modes of protein-protein interaction have contributed to the origin of the flower. The new advances have not only corrected some mistakes in previous theories and models, stimulated the proposal of new and testable hypotheses, but also revealed the contribution of the evolution of floral MADS-box genes to the origin of the flower. However, previous studies can only provide general explanations for how the flower as a whole originated, but are insufficient for a complete understanding of the underlying mechanisms of the origins of different floral organs. In this review, we summarize the theories and hypotheses explaining the origin of the flower and floral organs. On the basis of this framework, we provide the current understanding of the flower itself and its origin. In our opinion, changes of many “small” key characters have been involved in the origin of the flower and the establishment of its basic structure. We propose that elucidation of the mechanisms underlying the evolution of these characters is the prerequisite for understanding the intrinsic basis for the origin of the flower.