The vascular plants: open system of growth

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.

Redox regulation at the site of primary growth: auxin, cytokinin and ROS crosstalk

“…In addition to SAM and RAM, secondary meristematic tissues also contribute to plant developmental plasticity. We refer readers to excellent reviews on that topic, including those examining procambium formation and the control of cambium activity (Jouannet et al 2015), developmental processes of axillar initiation and outgrowth (Agusti & Greb 2013;Basile et al 2017) and thiol-based regulatory mechanisms controlling maintenance of plant meristems and floral development (Rouhier et al 2015;Schippers et al 2016).…”

Disentangling phylogenetic and functional components of shape variation among shoot apical meristems of a wide range of herbaceous angiosperms

“…First, the sunken type of the meristem is associated with thicker stems relative to plant height (see also Stant, ; Serebryakova, ). Stem cells arise from the rib zone of the meristem, which is involved in the building of vascular bundles, pith, and cortex (Mauseth, ; Basile et al., ). Because herbaceous plants do not have secondary growth, cell divisions directly under the meristem are responsible for the final anatomical structure of the stem and its thickness underlying the correlation of large, flat, and sunken meristems with thick stems.…”

“…The form and function of a plant is determined by the perpetual existence of meristematic tissue organized in shoot apical meristems (SAMs; Carraro et al., ; Nardmann et al., ; Basile et al., ). The interplay of individual meristem domains and molecular processes determines meristem size, shape, and structure that govern plant growth patterns and are responsible for initiation of leaf primordia, branching and stem arrangement (Bäurle and Laux, ; Tucker and Laux, ).…”

“…The interplay of individual meristem domains and molecular processes determines meristem size, shape, and structure that govern plant growth patterns and are responsible for initiation of leaf primordia, branching and stem arrangement (Bäurle and Laux, ; Tucker and Laux, ). Diverse traits such as phyllotaxy, leaf size, inflorescence structure, and stem internal organization (vascular bundles, pith, cortex, and epidermis) are directly determined by the shoot apical meristem (Bartlett and Thompson, ; Basile et al., ; Schnablová et al., ). Meristem structure thus constitutes a link among anatomical organization of plant organs and, consequently, functional traits that determine a plant's response to its environment and its ultimate ecological success.…”

“…The rib meristem is located below the organizing center and is composed of cells dividing in all directions. Its derivatives are involved in the organization of the stem and building of vascular bundles, pith, and cortex (Mauseth, ; Basile et al., ). The relationship of these functional domains, hormonal regulation, diverse gene expression, and mechanical cell wall properties determine the final SAM shape (Bowman and Eshed, ; Nardmann and Werr, ; Lian et al., ; Nardmann et al., ; Galli and Gallavotti, ).…”