Plant Organ Shapes Are Regulated by Protein Interactions and Associations With Microtubules

Abstract

Plant organ shape is determined by the spatial-temporal expression of genes that control the direction and rate of cell division and expansion, as well as the mechanical constraints provided by the rigid cell walls and surrounding cells. Despite the importance of organ morphology during the plant life cycle, the interplay of patterning genes with these mechanical constraints and the cytoskeleton is poorly understood. Shapes of harvestable plant organs such as fruits, leaves, seeds and tubers vary dramatically among, and within crop plants. Years of selection have led to the accumulation of mutations in genes regulating organ shapes, allowing us to identify new genetic and molecular components controlling morphology as well as the interactions among the proteins. Using tomato as a model, we discuss the interaction of Ovate Family Proteins (OFPs) with a subset of TONNEAU1-recruiting motif family of proteins (TRMs) as a part of the protein network that appears to be required for interactions with the microtubules leading to coordinated multicellular growth in plants. In addition, SUN and other members of the IQD family also exert their effects on organ shape by interacting with microtubules. In this review, we aim to illuminate the probable mechanistic aspects of organ growth mediated by OFP-TRM and SUN/IQD via their interactions with the cytoskeleton.

Keywords: IQD; OFP; SUN; TRM; microtubules; organ shape.

FIGURE 1

Preprophase band and organ shape. The positioning of the PPB marks the future site of cell division. The direction of cell division will greatly influence the shape of the emerging organ.

FIGURE 2

Effect of the fruit shape genes in the wild type tomato background. The loci were introgressed (sun, ovate, sov1) or edited (trm5) in the Solanum pimpinellifolium accession LA1589 background to create near isogenic lines (NILs). WT, wild type; sov1, suppressor of ovate corresponding to SlOFP20. The single natural NILs are shown on the top of the figure, whereas the double and triple NILs are shown below the single NILs.

FIGURE 3

Expression patterns of OVATE, SlOFP20, SlTRM5 and SUN during floral development. Samples were collected from wild-type S. pimpinellifolium LA1589 or the sun NIL in the LA1589 background. RPKM, reads per kilobase of transcript per million mapped reads; IM, inflorescence meristem; FM, floral meristem; dpi, flower buds collected in number of days post floral initiation. Each value represents 3 to 4 biological replicates, each containing 100–150 meristems or young flower buds. The bars indicate standard errors among the four replicates. The expression data is available under BioProject number PRJNA343236 and SRP089970 as well as on the Sol Genomics Network website (https://www.sgn.cornell.edu/) at the Tomato Functional Genomics Database (http://ted.bti.cornell.edu/cgi-bin/TFGD/digital/home.cgi).

FIGURE 4

A model of the regulation of plant organ shapes. Expression levels of OFP1-like, TRM1-5-like and SUN/IQD-like lead to more or less association with microtubules to determine organ shape. Red oval shape, OFP1-like; green oval shape, TRM1-5-like; blue bar, microtubule; orange circle, SUN/IQD-like; purple triangle, SPR2; pink square, calmodulin.