Localized growth and remodelling drives spongy mesophyll morphogenesis

Abstract

The spongy mesophyll is a complex, porous tissue found in plant leaves that enables carbon capture and provides mechanical stability. Unlike many other biological tissues, which remain confluent throughout development, the spongy mesophyll must develop from an initially confluent tissue into a tortuous network of cells with a large proportion of intercellular airspace. How the airspace in the spongy mesophyll develops while the tissue remains mechanically stable is unknown. Here, we use computer simulations of deformable polygons to develop a purely mechanical model for the development of the spongy mesophyll tissue. By stipulating that cell wall growth and remodelling occurs only near void space, our computational model is able to recapitulate spongy mesophyll development observed in Arabidopsis thaliana leaves. We find that robust generation of pore space in the spongy mesophyll requires a balance of cell growth, adhesion, stiffness and tissue pressure to ensure cell networks become porous yet maintain mechanical stability. The success of this mechanical model of morphogenesis suggests that simple physical principles can coordinate and drive the development of complex plant tissues like the spongy mesophyll.

Structural and Physiological Traits of Compound Leaves of Ceratonia siliqua Trees Grown in Urban and Suburban Ambient Conditions

“…Elevated values were estimated in samples of the NG site, probably because trees grown there are exposed to the air pollution emitted by continuous, diurnal traffic of cars. The leaf spongy mesophyll tissue enables carbon capture and provides mechanical stability; also, unlike many other biological tissues, which remain confluent throughout development, the spongy mesophyll develops from an initially confluent tissue into a network of cells with a relatively large proportion of intercellular airspace [ 59 ]. In addition, urban leaves possessed a significantly thicker thickness of both the adaxial and the abaxial epidermises, as well as the periclinal wall of adaxial and abaxial epidermal cells.…”

Flowers are leakier than leaves but cheaper to build

“…Although they are typically short-lived, flowers require resources, such as carbon, water, and nutrients, for their production and maintenance (Reekie & Bazzaz, 1987a,b;Ashman & Schoen, 1994;Song et al, 2022). Water, in particular, is needed throughout development and anthesis for a variety of functions, including driving growth and expansion, keeping flowers turgid and on display for pollinators, providing rewards such as nectar, and for regulating temperature (Bazzaz et al, 1987;Galen et al, 1999;Patiño & Grace, 2002;Chapotin et al, 2003;De la Barrera & Nobel, 2004;Roddy & Dawson, 2012;Roddy, 2019;Treado et al, 2022). Additionally, flowers regularly lose water to the atmosphere, and this water loss may increase during hot and dry conditions often associated with droughts (Hew et al, 1980;Feild et al, 2009;Teixido & Valladares, 2014;Sinha et al, 2022).…”

The effects of genome size on cell size and the functional composition and morphology of leaves: a case study inRhododendron(Ericaceae)

“…Because the leaf mesophyll is under pressure from the leaf epidermis, the biomechanical properties of the living mesophyll tissue is critical to the maintenance of a porous mesophyll capable of high rates of CO 2 diffusion (Théroux-Rancourt et al 2021). In fact (and somewhat counterintuitively), this positive pressure imposed by the epidermis combined with the positive turgor pressure of the mesophyll is vital for the development of mesophyll porosity during leaf morphogenesis (Treado et al 2022). Consistent with the role of mesophyll hydraulics in leaf biomechanics, leaves with low LMA shrink more during desiccation, suggesting that their high water contents are critical to their structural integrity (Scoffoni et al 2014).…”

“…Within leaves, cells are organized into tissues that must efficiently fill the leaf volume and accomplish multiple functions, including scattering and absorbing light, facilitating CO 2 diffusion into the mesophyll cells for photosynthesis, and remaining biomechanically robust (Smith et al 1997;Roderick, Berry, Saunders, et al 1999;Théroux-Rancourt et al 2021;Borsuk et al 2022;Treado et al 2022). None of these functions are performed solely by individual cells: leaf performance depends on the whole leaf, which is composed of multiple tissues and their constituent cells.…”