FW2.2 and cell cycle control in developing tomato fruit: a possible example of gene co-option in the evolution of a novel organ

Abstract

fw2.2 is one of the few QTLs thus far isolated from plants and the first one known to control fruit size. While it has been established that FW2.2 is a regulator (either directly or indirectly) of cell division, FW2.2 does not share sequence homology to any protein of known function (Frary et al. Science 289:85-88, 2000; Cong et al. Proc Natl Acad Sci USA 99:13606-13611, 2002; Liu et al. Plant Physiol 132:292-299, 2003). Thus, the mechanism by which FW2.2 mediates cell division in developing fruit is currently unknown. In an effort to remedy this situation, a combination of yeast two-hybrid screens, in vitro binding assays and cell bombardment studies were performed. The results provide strong evidence that FW2.2 physically interacts at or near the plasma membrane with the regulatory (beta) subunit of a CKII kinase. CKII kinases are well-studied in both yeast and animals where they form part of cell cycle related signaling pathway. Thus while FW2.2 is a plant-specific protein and regulates cell division in a specialized plant organ (fruit), it appears to participate in a cell-cycle control signal transduction pathway that predates the divergence of single- and multi-cellular organisms. These results thus provide a glimpse into how ancient and conserved regulatory processes can be co-opted in the evolution of novel organs such as fruit.

Tomato (Solanum lycopersicum L.) in the service of biotechnology

“…Therefore, some research has been conducted regarding to this fruit characteristic. Detailed studies on dosage series of the fw2.2 gene encoding plantspecific protein regulating cell divisions, particularly in fruits, were performed on transgenic tomatoes, allowing for fruit size to be altered (Liu et al 2003;Cong and Tanksley 2006). Since the detailed mechanism by which fw2.2 participates in fruit development is unknown, deciphering this enigma is one of the keys to understanding the phenomenon of fruit development.…”

“…Since the detailed mechanism by which fw2.2 participates in fruit development is unknown, deciphering this enigma is one of the keys to understanding the phenomenon of fruit development. Cong and Tanksley (2006) suggested that fw2.2 might have mediated this process through gene co-option and recruitment of a cell cycle control pathway. As it turns out, fw2.2 interacted with the highly conserved regulatory unit of CKII b ((beta) subunit of a CKII kinase) and thus may affect regulation of cell division via CKII mediated pathways.…”

Regulatory change at Physalis Organ Size 1 correlates to natural variation in tomatillo reproductive organ size

“…A mutation in the FW2.2 promoter resulted in fruit enlargement via heterochronic expression of the gene during fruit development [13][14][15] . FW2.2 is a plasma membrane-anchored protein, which is involved in the cell cycle pathway for ovary size control 16 . Another two cloned loci namely fasciated (fas) and locule number (lc) mainly control the locule number of ovary 17,18 .…”

Evolution of FW2.2-like (FWL) and PLAC8 genes in eukaryotes

“…Phenotypic observations of a LeFW2.2 gene dosage series in tomato plants 6 indicated an inverse relationship between fruit size and FW2.2 expression. Subsequently, yeast two-hybrid studies showed a direct interaction between LeFW2.2 and the β sub-unit of casein kinase II, 3 a broad specificity protein kinase previously shown to regulate the cell cycle. [7][8][9] These findings led to the hypothesis that LeFW2.2 controls fruit size through regulation of the cell cycle, perhaps mediated through direct interaction with casein kinase II.…”