Fruit Calcium: Transport and Physiology

Abstract

Calcium has well-documented roles in plant signaling, water relations and cell wall interactions. Significant research into how calcium impacts these individual processes in various tissues has been carried out; however, the influence of calcium on fruit ripening has not been thoroughly explored. Here, we review the current state of knowledge on how calcium may impact the development, physical traits and disease susceptibility of fruit through facilitating developmental and stress response signaling, stabilizing membranes, influencing water relations and modifying cell wall properties through cross-linking of de-esterified pectins. We explore the involvement of calcium in hormone signaling integral to the physiological mechanisms behind common disorders that have been associated with fruit calcium deficiency (e.g., blossom end rot in tomatoes or bitter pit in apples). This review works toward an improved understanding of how the many roles of calcium interact to influence fruit ripening, and proposes future research directions to fill knowledge gaps. Specifically, we focus mostly on grapes and present a model that integrates existing knowledge around these various functions of calcium in fruit, which provides a basis for understanding the physiological impacts of sub-optimal calcium nutrition in grapes. Calcium accumulation and distribution in fruit is shown to be highly dependent on water delivery and cell wall interactions in the apoplasm. Localized calcium deficiencies observed in particular species or varieties can result from differences in xylem morphology, fruit water relations and pectin composition, and can cause leaky membranes, irregular cell wall softening, impaired hormonal signaling and aberrant fruit development. We propose that the role of apoplasmic calcium-pectin crosslinking, particularly in the xylem, is an understudied area that may have a key influence on fruit water relations. Furthermore, we believe that improved knowledge of the calcium-regulated signaling pathways that control ripening would assist in addressing calcium deficiency disorders and improving fruit pathogen resistance.

Keywords: calcium; fruit ripening; pectin; water; xylem.

FIGURE 1

Several major components determine calcium supply and distribution in fruit. Calcium is phloem immobile, accumulating through the xylem. Hydraulic factors, particularly fruit water uptake and loss driven by cell expansion and transpiration largely determine the volume of xylem fluid supplied to the fruit (A). Physical properties of the xylem, including xylem vessel development, vessel diameter and connectivity will influence xylem flow into different tissues of the fruit (B). Structural properties of the cell wall, both in xylem vessels and fruit mesocarp and epidermal tissues, can affect the rate of xylem flow and calcium binding in these compartments (C). Pectin is a major component of fruit cell walls; de-esterification of pectin enables formation of calcium crosslinked gels affecting pit membrane porosity, xylem flows and calcium distribution. Additionally, tight regulation of cytosolic calcium concentration occurs through a network of membrane transporters on the plasma membrane and tonoplast, including aquaporins, Ca²⁺-ATPases and CAX ion channels (D). These transport mechanisms can enable accumulation of calcium in particular tissues.

FIGURE 2

Cell wall changes and calcium-pectin crosslink formation affects fruit mechanical properties, water relations and pathogen susceptibility. Upregulation of cell wall modifying and hydraulic regulatory genes (e.g., pectin methyl esterases, polygalacturonases, and aquaporins) occurs in the mesocarp at veraison. The majority of pectins occur in the middle lamella, with smaller amounts observed in the primary cell wall. Localization of calcium in particular extracellular domains is hypothesized to affect cell wall loosening and cell separation. This may be particularly relevant at three way cell junctions where turgor pressure is driving the separation of cells and the formation of large intra-cellular spaces. Cuticle composition is an important variable in determining both fruit physical properties and transpiration water losses throughout berry development. Processes affecting polysaccharide solubilisation and movement into the cuticle, such as pectin de-esterification and calcium crosslinking, and production of oligogalacturonides will modify fruit mechanical properties and pathogen susceptibility.