ANGUSTIFOLIA3 Signaling Coordinates Proliferation between Clonally Distinct Cells in Leaves

Abstract

Coordinated proliferation between clonally distinct cells via inter-cell-layer signaling largely determines the size and shape of plant organs. Nonetheless, the signaling mechanism underlying this coordination in leaves remains elusive because of a lack of understanding of the signaling molecule (or molecules) involved. ANGUSTIFOLIA3 (AN3, also called GRF-INTERACTING FACTOR1) encodes a putative transcriptional coactivator with homology to human synovial sarcoma translocation protein. AN3 transcripts accumulate in mesophyll cells but are not detectable in leaf epidermal cells. However, we found here that in addition to mesophyll cells, epidermal cells of an3 leaves show defective proliferation. This spatial difference between the accumulation pattern of AN3 transcripts and an3 leaf phenotype is explained by AN3 protein movement across cell layers. AN3 moves into epidermal cells after being synthesized within mesophyll cells and helps control epidermal cell proliferation. Interference with AN3 movement results in abnormal leaf size and shape, indicating that AN3 signaling is indispensable for normal leaf development. AN3 movement does not require type II chaperonin activity, which is needed for movement of some mobile proteins. Taking these findings together, we present a novel model emphasizing the role of mesophyll cells as a signaling source coordinating proliferation between clonally independent leaf cells.

Leaf Development

“…The mRNA expression domain of the AN3/ AtGIF1 is, however, restricted to inner tissue but not in epidermis in the leaf primordia (Kawade et al 2013). Detailed analyses of the an3 mutant showed that both the epidermis and inner tissue are under a control of the AN3/AtGIF1 activity, in terms of number of cells.…”

“…The apical part of the leaf primordium is occupied by small, non-polarized cells with longitudinal, transverse, and oblique arrangements of crosswalls relative to the proximal-distal axis. The basal part of the leaf primordium has large, longitudinally polarized cells that are arranged paral- protein moves from inner tissue to epidermis thereby coordinating cell proliferation between different tissue layers; interference with AN3 movement results in abnormal leaf size and shape, indicating that AN3 signaling is indispensable for normal leaf development with a coordinated growth between epidermis and inner tissue (Kawade et al 2013). This is the first report on the importance of the role of mesophyll layers as a signaling source for the coordinated cell proliferation in a leaf primordium.…”

“…Rather, lossof-function in AN3 specifically affects cell proliferation activity in phase II mitosis when longitudinal and oblique divisions increase at the expense of transverse divisions that are dominant in the earlier phase (phase I) (Horiguchi et al 2011a). AN3 regulates not only coordinated cell proliferation activity among tissue layers of leaf primordia by its intercellular movement (Kawade et al 2013), but also dorsiventrality of leaves (Horiguchi et al 2005;2011a) and the identity of cotyledons through suppression of expansion in the expression domain of PLETHORA1 (PLT1; AT3G20840) The molecular roles of genes other than ROT3 and AN3 in leaf morphogenesis remain enigmatic. AN is a member of Cterminal Binding Protein (CtBP)/Brefeldin-A-ADP ribosylated substrate (BARS), for which we have only an incomplete understanding (Chinnadurai 2006).…”

Leaf development and morphogenesis

“…Lamina growth also requires coordination between the epidermis and the mesophyll layers, and it was recently shown that the transcriptional co-activator ANGUSTIFOLIA3 (AN3) is produced only in mesophyll cells but moves into the epidermis to promote growth in both layers (Kawade et al, 2013). AN3 was subsequently shown to modulate transcription through interaction with chromatinremodeling factors (Vercruyssen et al, 2014).…”

Roles of the vacuolar H⁺-PPase in seed storage oil mobilization and plant development

“…For example, by considering the manner through which a cell reaches its ultimate size and performing kinematic analyses of cell size dynamism, three classes of compensation have been identified: Class I, an enhanced postmitotic cell expansion rate (seen in angustifolia [an]3-4, fugu2-1/fasciata [fas]1-5, and erecta [er]-102); Class II, an extended post-mitotic cell expansion period (seen in fugu5-1); and Class III, increase in the size of dividing cells (seen in KIP-RELATED PROTEIN 2 [KRP2] over-expressing cells) (Ferjani et al 2007(Ferjani et al , 2008(Ferjani et al , 2010(Ferjani et al , 2013a(Ferjani et al , 2013b(Ferjani et al , 2014. Furthermore, during compensation, cell-autonomous and non-cell-autonomous pathways have been identified (Kawade et al 2010, 2013, Ferjani et al 2013a. Finally, the fact that compensation occurs in a wide range of plant species other than Arabidopsis, including tobacco, rice, and snapdragon, suggests that common developmental mechanisms that trigger compensation are widely conserved in angiosperms (Hemerly et al 1995, Barrôco et al 2006, Delgado-Benarroch et al 2009.…”