Not another round: microtubule-associated proteins and the control of fruit shape in tomato

Fruits with extravagant shapes are attractive to consumers.Buda-shaped pears or Japanese square-shaped watermelons are extreme examples that are produced by restricting fruit growth during development.At the molecular level, the final shape of a fruit is determined partly by the number of locules through the regulation of genes controlling carpel initiation (e.g., WUSCHEL, FASCIATED, LOCULE NUMBER).Fruit shape also relies on controlled cell division and expansion patterns regulated by, e.g., OVATE FAMILY PROTEIN 20 or SUN1 (van der Knaap et al. 2014).SUN1, which is particularly important for fruit expansion localizes to the microtubules and affects microtubule organization and cell division in several species (Xiao et al. 2008; Bürstenbinder et al. 2017).Microtubule-associated proteins (MAPs) regulate cell growth and processes related to morphogenesis.However, it is not clear how MAPs regulate cell morphology and organ shape during reproductive development.In this issue, Zhiru Bao and colleagues (Bao et al. 2023) report the identification of MICROTUBULE ASSOCIATED PROTEIN 70-1 (MAP70-1), MAP70-2, and the IQ67-domain protein IQD21a as regulators of fruit shape that orchestrate microtubule dynamics involved in defining long, round, or flat tomato fruits.The authors studied the MAP70 proteins in tomato (Solanum lycopersicum), a group of five plant-specific microtubule-related proteins that localize to microtubules; SlMAP70-1 was chosen for further analysis since it has a higher expression during fruit development.The overexpression of SlMAP70-1 generated elongated fruits, while the knock-down lines generated short and flat ones (see Figure ).The slmap70-1 and slmap70-2 knock-out lines resulted in short fruits, and fruits were even shorter in the double mutant slmap70-1/2.At the cellular level, the SlMAP70 lines displayed contrasting features of microtubule organization.The SlMAP70 overexpression lines showed reduced cell circularity values (complex shapes), while the cells were more circular in the knockdown lines.Although the lobe number of the cells was not affected, the lobe length was shorter in the knock-down or knock-out lines and longer in the overexpression lines.The authors used live-cell imaging in the endocarp (a fruit tissue) to track the microtubule organization and dynamics.Anisotropy values (reflecting order in the microtubule filaments) in endocarp cells were similar from -3 to 0 days after pollination; after that, a dramatic re-orientation of the microtubules occurred.However, in the slmap70-1/2 double mutant, this re-arrangement was affected and the order in the microtubule filaments remained similar until anthesis and after pollination.Thus microtubule re-arrangement mediated by the SlMAP70 proteins at early stages may be crucial for organizing cell morphogenesis and the final fruit shape.To identify other microtubule-related proteins controlling fruit shape, a yeast two-hybrid assay was performed using SlMAP70-1 as bait; SlIQD21a (SUN10) was identified as a putative interaction partner.The IQD family has 33 members in tomato and several were selected to generate overexpression lines.The overexpression of SlIQD1 generated extremely elongated fruits; the effect of SlIQD21a was similar to SlMAP70-1 suggesting a cooperative function.The combined overexpression of SlMAP70-1 and SlIQD21a further enhanced fruit elongation.Analysis of cell features in these additional lines indicated anisotropy in microtubules increased in the mutant line slmap70-1/2 and reduced in the SlMAP70-1 overexpression line.Long fruits (overexpression of SLMAP70-1 or SlIQD21a) correlated with reduced cell circularity.In Arabidopsis pavement cells, high circularity correlates with low microtubule anisotropy, and cells expand