Tempting Fate: A Guanylate-Binding Protein Maintains Tomato Fruit Cell Differentiation.

Tissues are composed of specialized cell types. As a cell matures, it acquires the characteristics associated with a specific identity, or fate. This process is called cell differentiation and is crucial for proper organ development. However, after a differentiation program is initiated, the mechanisms underlying its maintenance are often unclear. In this issue of The Plant Cell, identified a new regulatory pathway that underlies cell fate maintenance in the fleshy fruit of tomato (Solanum lycopersicum).

As a fruit develops, cells divide during early growth and enlarge during late growth before ripening (Renaudin et al., 2017). Tomato pericarp tissue acquires fleshy properties due to water and solute accumulation in enlarging mesocarp cells (see figure). Mesocarp enlargement is also associated with endoreduplication, the replication of the nuclear genome in the absence of mitosis. To understand how these cell maturation programs are regulated, Musseau et al. (2017) characterized a tomato mutant isolated from a forward genetic screen.

Abnormal Pericarp Phenotype of Tomato gbp1 Fruit at the Breaker Stage.

Compared with the wild type (WT), gbp1 fruit has a thin pericarp (P) made up of disorganized cells. En, endocarp; Ex, exocarp; M, mesocarp; VB, vascular bundles.

(Adapted from , Figure 1.)

Compared with wild type, the mutant exhibited reduced pericarp thickness (see figure) but had no difference in the early production of pericarp layers, suggesting that late developmental events were affected. Mapping by sequencing indicated that a mutation in a gene encoding a GTPase guanylate binding protein (GBP), SlGBP1, caused the abnormal pericarp phenotype. Although GBPs have been described in humans and animals, their function in plants is poorly understood.

To determine how the mutant phenotype develops, the authors examined gbp1 fruit along a developmental time course. A higher proportion of small cells in the mesocarp suggested that the increase in cell expansion rate that normally takes place during the latter stages of development, beginning 20 d after a flower opens (days post anthesis; DPA), did not occur in gbp1 fruit.

Given that variations in tomato pericarp cell size are generally correlated with endoreduplication, the authors examined the nuclear ploidy levels of gbp1 pericarp cells. The ploidy index beginning at 20 DPA was much lower in the mutant compared to the wild type. Overall, the timing of endoreduplication was unaffected in gbp1 but a high proportion of cells stopped endocycling at a low ploidy state, suggesting that the process may be less efficient.

Another key factor that determines plant cell size and shape is cell wall rigidity. To examine cell wall differences between the wild type and gbp1, the authors examined the distribution and composition of pectins during fruit development. Together, the analyses suggested that cell wall loosening that takes place during wild-type fruit growth and ripening does not progress normally in gbp1 mesocarp. Comparison of metabolites between wild-type and gbp1 fruit pericarps also suggested that ripe gbp1 fruit is similar to developing wild-type fruit before ripening.

In addition to changes in wall composition, new cell walls formed themselves after 20 DPA in gbp1, which resulted from divisions of large mesocarp cells. Changes in temporal expression patterns of known endocycle and mitotic cycle regulators further supported the notion that cell division activity resumed during late gbp1 fruit growth at the expense of endoreduplication.

It is generally accepted that entrance into the endocycle marks the start of cell differentiation. However, polyploid mesocarp cells of the gbp1 mutant deviate from this developmental program and exhibit cell divisions during late stages of fruit growth. Thus, SlGBP1 may be an inhibitor of cell division, a function comparable to that of human hGBP-1 protein. These results reveal a previously unknown role for GBPs in the control of cell cycle genes in plants. Taken together, Musseau et al. (2020) identified a new fate maintenance pathway that is required for proper cell differentiation and organ development.