MACROCALYX and JOINTLESS Interact in the Transcriptional Regulation of Tomato Fruit Abscission Zone Development    

Abstract

Abscission in plants is a crucial process used to shed organs such as leaves, flowers, and fruits when they are senescent, damaged, or mature. Abscission occurs at predetermined positions called abscission zones (AZs). Although the regulation of fruit abscission is essential for agriculture, the developmental mechanisms remain unclear. Here, we describe a novel transcription factor regulating the development of tomato (Solanum lycopersicum) pedicel AZs. We found that the development of tomato pedicel AZs requires the gene MACROCALYX (MC), which was previously identified as a sepal size regulator and encodes a MADS-box transcription factor. MC has significant sequence similarity to Arabidopsis (Arabidopsis thaliana) FRUITFULL, which is involved in the regulation of fruit dehiscent zone development. The MC protein interacted physically with another MADS-box protein, JOINTLESS, which is known as a regulator of fruit abscission; the resulting heterodimer acquired a specific DNA-binding activity. Transcriptome analyses of pedicels at the preabscission stage revealed that the expression of the genes involved in phytohormone-related functions, cell wall modifications, fatty acid metabolism, and transcription factors is regulated by MC and JOINTLESS. The regulated genes include homologs of Arabidopsis WUSCHEL, REGULATOR OF AXILLARY MERISTEMS, CUP-SHAPED COTYLEDON, and LATERAL SUPPRESSOR. These Arabidopsis genes encode well-characterized transcription factors regulating meristem maintenance, axillary meristem development, and boundary formation in plant tissues. The tomato homologs were specifically expressed in AZs but not in other pedicel tissues, suggesting that these transcription factors may play key roles in pedicel AZ development.

Molecular mechanisms controlling plant organ abscission

“…In addition, GOB may act to keep pedicel AZ cells small as the Arabidopsis homolog (CUC2) does (Peaucelle et al 2007). Similar to SAM cells, tomato pedicel AZ cells also are competent to develop adventitious shoots (Nakano et al 2012), suggesting that LeWUS activity may affect the fates of the AZ cells, acting in a similar fashion to the Arabidopsis homolog, which regulates stem cell activity in SAMs (Mayer et al 1998). In addition, Arabidopsis KNAT1/BP, which acts in SAMs, determines the timing of floral abscission by restricting AZ cell size and number (Shi et al 2011).…”

“…Intriguingly, the set of identified genes included several TF genes whose homologs are involved in meristem cell fates, including LeWUS, GOBLET (GOB), Ls, and Blind (Bl), which are identical to the genes expressed in SAMs of tomato seedlings. These four genes are expressed in pedicel AZs, not in the surrounding pedicel regions (Figure 2; Nakano et al 2012), suggesting their involvement in AZ function. LeWUS is a homolog of Arabidopsis WUSCHEL (WUS), which encodes a homeodomain family TF and plays a critical role in the maintenance of SAMs (Mayer et al 1998;Reinhardt et al 2003).…”

“…Among the several genes identified in the sequenced region, a gene for C-terminal domain phosphatase-like1 (ToCPL1) is a candidate for the j2 gene (Yang et al 2005). In addition, a recent study using antisense suppression showed that MACROCALYX (MC), a tomato APETALA1 family MADS-box gene, is also required for pedicel AZ formation (Nakano et al 2012). The study also found that MC and JOINTLESS can form a heterodimer that binds to a DNA motif, the CArG-box, which is known as the target of MADS-box TFs, suggesting that MC regulates pedicel AZ differentiation via forming a MADS-box complex with JOINTLESS.…”

“…The j and j2 mutations completely block the differentiation of the AZ and thus mutant plants develop AZ-less pedicels. The ls mutant was originally found as a lateral shoot-lacking plant, and was also found to develop incomplete pedicels (Nakano et al 2012;Roberts et al 2002). Molecular cloning revealed that JOINTLESS encodes a MADSbox TF and Ls encodes a GARS family TF (Mao et al 2000;Schumacher et al 1999).…”

“…A survey of the genes down-regulated by a defect in MC or JOINTLESS (Nakano et al 2012) revealed another aspect of the regulation of organ abscission. Intriguingly, the set of identified genes included several TF genes whose homologs are involved in meristem cell fates, including LeWUS, GOBLET (GOB), Ls, and Blind (Bl), which are identical to the genes expressed in SAMs of tomato seedlings.…”