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The Influence of Cell Wall Composition on Flower Development and Reproduction

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The Influence of Cell Wall Composition on Flower Development and Reproduction G C A T T A C G G C A T genes Review Building a Flower: The Influence of Cell Wall Composition on Flower Development and Reproduction José Erik Cruz-Valderrama, Judith Jazmin Bernal-Gallardo, Humberto Herrera-Ubaldo and Stefan de Folter * Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV-IPN), Unidad de Genómica Avanzada (UGA-LANGEBIO), Irapuato CP 36824, Guanajuato, Mexico; [email protected] (J.E.C.-V.); [email protected] (J.J.B.-G.); [email protected] (H.H.-U.) * Correspondence: [email protected] Abstract: Floral patterning is a complex task. Various organs and tissues must be formed to fulfill reproductive functions. Flower development has been studied, mainly looking for master regulators. However, downstream changes such as the cell wall composition are relevant since they allow cells to divide, differentiate, and grow. In this review, we focus on the main components of the primary cell wall—cellulose, hemicellulose, and pectins—to describe how enzymes involved in the biosynthesis, modifications, and degradation of cell wall components are related to the formation of the floral organs. Additionally, internal and external stimuli participate in the genetic regulation that modulates the activity of cell wall remodeling proteins. Keywords: flower development; cell wall; remodeling enzymes; cellulose; hemicellulose; pectin Citation: Cruz-Valderrama, J.E.; Bernal-Gallardo, J.J.; Herrera-Ubaldo, H.; de Folter, S. Building a Flower: 1. Introduction The Influence of Cell Wall The process of flower development involves the formation of very complex structures. Composition on Flower Development Flowers generally arise from the inflorescence meristem, where cellular differentiation and Reproduction. Genes 2021, 12, processes give rise to specialized structures involved in all the aspects of plant reproduction. 978. https://doi.org/10.3390/ Once the flower primordium is formed, specific changes can be observed in this area; genes12070978 cell growth, division, and differentiation make up tissues with different identities and functions [1]. A large part of the angiosperms shows a relatively conserved arrangement of Academic Editor: Christian Chevalier the floral whorls (Figure1). From the inside out, we can find the gynoecium, the female structure of the flower which houses the ovules, surrounded by the androecium, the male Received: 30 May 2021 part of the flower, represented by the stamens and, where pollen grains are produced. The Accepted: 23 June 2021 corolla, made up of vegetative structures that present a wide range of colors, helping to Published: 26 June 2021 attract specific pollinators, and the most outside whorl is the calyx, where the sepals protect the floral structures formed towards the center of the flower [2,3]. The formation of each Publisher’s Note: MDPI stays neutral whorl involves specific changes at the cellular level where cell division, expansion, and with regard to jurisdictional claims in published maps and institutional affil- cell death intervene finely to generate the female and male gametes that will eventually iations. come together in the fertilization process, giving origin to the seeds that ensure the next generation of plants (Figure1). Flower development has been finely described for plant species such as Arabidopsis, Petunia, and Antirrhinum. For these species, several genes (most of them transcription factors) are known to guide the differentiation of the floral whorls [1,4]. Knowledge from these model species suggests that at the molecular level, Copyright: © 2021 by the authors. there is a core mechanism that is conserved across the great variety of flowering plants [5]. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). Genes 2021, 12, 978. https://doi.org/10.3390/genes12070978 https://www.mdpi.com/journal/genes Genes 2021, 12, x FOR PEER REVIEW 2 of 17 Genes 2021, 12, 978 2 of 16 Figure 1. Flower development is related to cellular processes where the cell wall actively participates. In the earliest stages Figure 1. Flower development is related to cellular processes where the cell wall actively partici- of flower development, cell proliferation is highly active. Up to Stage 3 of floral development, it can be seen how the pates. In the earliest stages of flower development, cell proliferation is highly active. Up to Stage 3 calyx is already shown in the shape of a primordium, differentiated from the central structure that will give rise to the of floral development, it can be seen how the calyx is already shown in the shape of a primordium, other threedifferentiated flower whorls. from Cell the proliferation central structure and differentiation that will give processes rise to the are other essential three in flower these whorls. steps, where Cell the cell wall is actively involved.proliferation In Stage and 6, differentiation the structures processes of the already are essential differentiated in these floral steps, whorls where are the conspicuously cell wall is ac- observed, where the sepals alreadytively involved. cover the In innermost Stage 6, the structures. structures Later of the in Stagealready 8, thedifferentiated marginal meristem floral whorls of the are carpel conspicu- is a structure that is already presentously andobserved, will give where rise tothe tissues sepals such already as the cover placenta the innermost and ovules. structures. For Stage Later 9, a shapedin Stage septum 8, the mar- can be perfectly recognized.ginal At Stagemeristem 12, theof the style carpel and is transmitting a structure tractthat is are already differentiated present and as well will asgive the rise valves, to tissues and thesuch margins of the valves beginas the to be placenta morphologically and ovules. distinct. For Stage The 9, a petals shaped and septum the stamens can be areperfect structuresly recognized. where theAt S cellulartage 12, expansion is determinantthe for style the and growth transmitting of the organs. tract Inare Stage differentiated 13, the gynoecium as well as is the fully valves, developed, and the with margins anthesis of the and self-pollination valves begin to be morphologically distinct. The petals and the stamens are structures where the of the flower taking place. Programmed cell death is detected in the abscission zones where the organs open first by the cellular expansion is determinant for the growth of the organs. In Stage 13, the gynoecium is fully separation of the cells. developed, with anthesis and self-pollination of the flower taking place. Programmed cell death is detected in the abscission zones where the organs open first by the separation of the cells. The involvement of cell wall-related genes has been described during plant develop- ment. The detection of different cell wall components in different plant organs, including The involvement of cell wall-related genes has been described during plant develop- roots, leaves, stems, and flowers has been reported [6]. In addition, work has been per- ment. The detection of different cell wall components in different plant organs, including formed analyzing cell wall composition and dynamics during carpel medial domain roots, leaves, stems, and flowers has been reported [6]. In addition, work has been per- development [7]. The plant cell wall is a dynamic structure composed mainly of three formed analyzingtypes cell of wall polysaccharides: composition and cellulose, dynamics hemicelluloses, during carpel and medial pectins. domain These de- polymers interact velopment [7]. Theand plant assemble cell wall to constitute is a dynamic a network structure with composed structural proteinsmainly of that three are types inserted in a gel-like of polysaccharides:matrix cellulose, through hemicelluloses, different types and of chemicalpectins. These bonds polymers and physical interact arrangements and [8]. This assemble to constitutearchitecture a network allows with plant structural cells to maintain proteins a definedthat are shape, inserted confer in a mechanical gel-like support, and matrix through keepdifferent intercellular types of communicationchemical bonds and in the physical different arrangements organs. The [8]. composition This ar- and chemical chitecture allowsstructure plant cells of theseto maintain polysaccharides a defined mayshape change, confer during mechanical plant support, development and in response to keep intercellularenvironmental communication and in endogenous the different signals organs. [9]. The composition ofand the chemical cell wall varies depend- structure of theseing polysaccharides on the species, themay cell change type, during and even plant the development subcellular domain in response within to the cell wall of environmental oneand singleendogenous cell [9]. signals This variation [9]. The incomp the contentosition of suggests the cell that wall the varies plant de- cell wall is highly pending on the dynamicspecies, the and cell can type, be modulated and even the in quitesubcellular specific domain ways. Thewithin cell the wall cell plays wall an essential role of one single cellin [9]. the This morphogenesis variation in ofthe plants. content As suggests mentioned that above, the plant gene cell regulatory wall is highly networks underlying dynamic and canthe be differentiation modulated in quite of the specific floral meristem ways. The and cell floral
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