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The vascular plants: open system of growth

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Abstract

What is fascinating in plants (true also in sessile animals such as corals and hydroids) is definitely their open and indeterminate growth, as a result of meristematic activity. Plants as well as animals are characterized by a multicellular organization, with which they share a common set of genes inherited from a common eukaryotic ancestor; nevertheless, circa 1.5 billion years of evolutionary history made the two kingdoms very different in their own developmental biology. Flowering plants, also known as angiosperms, arose during the Cretaceous Period (145–65 million years ago), and up to date, they count around 235,000 species, representing the largest and most diverse group within the plant kingdom. One of the foundations of their success relies on the plant–pollinator relationship, essentially unique to angiosperms that pushed large speciation in both plants and insects and on the presence of the carpel, the structure devoted to seed enclosure. A seed represents the main organ preserving the genetic information of a plant; during embryogenesis, the primary axis of development is established by two groups of pluripotent cells: the shoot apical meristem (SAM), responsible for gene rating all aboveground organs, and the root apical meristem (RAM), responsible for producing all underground organs. During postembryonic shoot development, axillary meristem (AM) initiation and outgrowth are responsible for producing all secondary axes of growth including inflorescence branches or flowers. The production of AMs is tightly linked to the production of leaves and their separation from SAM. As leaf primordia are formed on the flanks of the SAM, a region between the apex and the developing organ is established and referred to as boundary zone. Interaction between hormones and the gene network in the boundary zone is fundamental for AM initiation. AMs only develop at the adaxial base of the leaf; thus, AM initiation is also strictly associated with leaf polarity. AMs function as new SAMs: form axillary buds with a few leaves and then the buds can either stay dormant or develop into shoot branches to define a plant architecture, which in turn affects assimilate production and reproductive efficiency. Therefore, the radiation of angiosperms was accompanied by a huge diversification in growth forms that determine an enormous morphological plasticity helping plants to environmental changes. In this review, we focused on the developmental processes of AM initiation and outgrowth. In particular, we summarized the primary growth of SAM, the key role of positional signals for AM initiation, and the dissection of molecular players involved in AM initiation and outgrowth. Finally, the interaction between phytohormone signals and gene regulatory network controlling AM development was discussed.

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Acknowledgements

This work was supported by the Università degli Studi di Pisa.

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Authors and Affiliations

  1. Institute of Biology, RWTH Aachen University, Aachen, Germany

    Alice Basile

  2. Dipartimento di Scienze Agrarie, Ambientali e Agro-alimentari, Università degli Studi di Pisa, Pisa, Italy

    Marco Fambrini & Claudio Pugliesi

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  1. Alice Basile
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Communicated by Sureshkumar Balasubramanian

“In opposition to animals, vascular plants form an open system in which growth is localized in embryonic areas, the meristems, which all along individual life form new tissues and organs which are added to those formed during embryogenesis (D’Amato 1964).” For this developmental characteristic, plants have sometimes been defined as organisms with continued embryogenesis (Bower 1930) or recurrent ontogenesis (Chiarugi 1952). The shoot apical meristem acts as a reservoir of the genetic information of the plant which is directly delivered to the mega- and microsporogeneous tissues (germline) at time of change of the apical meristem from the vegetative to the reproductive phase (D’Amato 1977, 1997).

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Basile, A., Fambrini, M. & Pugliesi, C. The vascular plants: open system of growth. Dev Genes Evol 227, 129–157 (2017). https://doi.org/10.1007/s00427-016-0572-1

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