Fusoid cells in the grass family Poaceae (Poales): a developmental study reveals homologies and suggests new insights into their functional role in young leaves

Abstract

Background and Aims In mature grass leaf blades as seen in cross-section, oblong cell-like structures have been interpreted most recently as intercellular gas spaces delimited by successive collapsed fusoid cells. These cells have been reported in at least seven of 12 subfamilies of Poaceae and are considered a synapomorphy for the family; however, no developmental work has been performed to verify their meristematic origin or to assess possible homologies within the graminid clade (= Flagellariaceae + [(Joinvilleaceae + Ecdeiocoleaceae) + Poaceae]) or among subfamilies of Poaceae. A developmental study was therefore carried out, including 20 species in three families (Flagellariaceae, Joinvilleaceae and Poaceae), representing the earlier-diverging and derived branches within the graminid clade and Poaceae. • Methods Light microscopy was combined with scanning electron microscopy, cryoscanning electron microscopy and transmission electron microscopy to study the development of leaves taken from the shoot apex of young plants. Mature leaf blades also were taken from living or dried plants and the mid-portion was studied. • Key Results Developmental results show that, in mature leaf blades as seen in cross-section, one apparent fusoid cell is typically a cavity resulting from the collapse of the initial fusoid cell and its internal divisions, which are herein interpreted as derivative cells with formation of cell plates only. Each cavity is delimited by successive collapsed fusoid cells arranged perpendicularly to the veins. Fusoid cells in all studied Poaceae members originate from the ground meristem, as do the colourless cells in Joinvillea ascendens (Joinvilleaceae). These two types of mesophyll cell have a strongly similar ontogeny, distinguished mainly by the collapse of the fusoid cells in Poaceae, which is not observed in the colourless cells in J. ascendens. • Conclusions Within the Poaceae, the meristematic origin of fusoid cells is the same in the early-diverging lineages, BOP clade and Panicoideae, and thus they are homologous within the family. The same topography and meristematic origin suggest that fusoid cells in Poaceae and colourless cells in Joinvilleaceae are homologous. The results also suggest that the role played by the fusoid cells in young grass leaves is related to synthesis and storage of starch granules at early stages of development.

The botanical multiverse of Peter Barlow

“…In all examined taxa of the Poaceae, fusoid cells originate from the ground meristem, as do the colourless cells in Joinvillea ascendens (Joinvilleaceae), and both these types of mesophyll cells have a strongly similar ontogeny suggesting that they are homologous. Leandro et al also present results suggesting that, at least in young grass leaves, fusoid cells play a role related to synthesis and storage of starch granules at early stages of development [27].…”

“…But, this 'left-of-field' sort of study brings to mind Peter's own seemingly off-kilter work on the developmental anatomy of Ginkgo [29], which develops curious downgrowthsknown as chi-chifrom aerial parts of the stem. As with Leandro et al fusoid cell study [27] and the relevance of those structures to photorespiration [30] or partitioning of photosynthate within cells of grass leaves and cereal crops more specifically, Barlow & Kurczyńska's study [29] provides an anatomical and developmental study which gave insights into a mode of elongation growth that is an alternative to that which is usually considered to be the preserve of apical meristems.…”

“…Grasses are also well-catered for -Zea mays was a favoured experimental organism of Peter's, which he used many times during his career (for such work as ultrastructural study of its quiescent centre [21], endoreduplication in metaxylem cells [22], root morphogenesis [23], cytoskeleton studies [24], gravitropism [25], and investigations of the impedance of soils to root growth [26]). Appropriately, in the SIAB, we have developmental study of fusoid cells in grass leaves [27], and the review of cross-talk between cells during formation of the subsidiary cells in maize [28].…”

“…Leandro et al [27] investigate fusoid cells, important features of the blade of certain grass species, but which, despite having acknowledged systematic value, are little understood structures in terms of their taxonomic distribution amongst the Poaceae and their functional role within the grass leaf. Using detailed microscopic investigations the authors chart the development of these features in 20 species in three families -Poaceae, Flagellariaceae, and Joinvilleaceae (the latter two representing the earlier diverging and derived branches within the Graminid clade and Poaceae).…”

“…At first sight, this study [27] is of a topic which may seem arcane, and of limited relevance to real-world concerns. But, this 'left-of-field' sort of study brings to mind Peter's own seemingly off-kilter work on the developmental anatomy of Ginkgo [29], which develops curious downgrowthsknown as chi-chifrom aerial parts of the stem.…”