Specification of adaxial cell fate during maize leaf development

Abstract

Dorsoventral (adaxial/abaxial) polarity of the maize leaf is established in the meristem and is maintained throughout organ development to coordinate proper outgrowth and patterning of the leaf. rolled leaf1(rld1) and leafbladeless1 (lbl1) are required for the specification of the adaxial/upper leaf surface. rld1 encodes a class III homeodomain-leucine zipper (HD-ZIPIII) protein whose adaxial expression is spatially defined by miRNA166-directed transcript cleavage on the abaxial side. The semi-dominant Rld1-Original (Rld1-O)mutation, which results from a single nucleotide substitution in the miRNA166 complementary site, leads to persistent expression of mutant transcripts on the abaxial site. This causes the adaxialization or partial reversal of leaf polarity. By contrast, recessive mutations in lbl1 cause the formation of abaxialized leaves. The lbl1 and Rld1-Omutations mutually suppress each other, indicating that these two genes act in the same genetic pathway. Adaxial and meristematic expression of rld1is reduced in lbl1 mutants, indicating that lbl1 acts upstream of rld1 to specify adaxial fate during primordium development. However, rld1 expression in the vasculature of lbl1 is normal, suggesting that the specification of adaxial/abaxial polarity during vascular and primordia development is governed by separate but overlapping pathways. We also show that members of the maize yabbygene family are expressed on the adaxial side of incipient and developing leaf primordia. This expression pattern is unlike that observed in Arabidopsis, where YABBY expression is correlated with abaxial cell fate. The yabby expression patterns in lbl1 and Rld1-O mutants suggest that the yabby genes act downstream in the same pathway as lbl1 and rld1. Moreover, our observations suggest that maize yabby genes may direct lateral organ outgrowth rather than determine cell fate. We propose that a single genetic pathway involving lbl1, rld1 and the yabby genes integrates positional information within the SAM, and leads to adaxial/abaxial patterning and mediolateral outgrowth of the leaf.

Transcriptomic Analyses Indicate That Maize Ligule Development Recapitulates Gene Expression Patterns That Occur during Lateral Organ Initiation

“…ns1 encodes a WUSCHEL-LIKE HOMEOBOX3 protein that is required for recruitment of lateral leaf founder cells during early stages of maize leaf development (Scanlon et al, 1996;Nardmann et al, 2004). At least two Class III HOMEODOMAIN LEUCINE ZIPPER (HD-ZIPIII) genes with homology to the Arabidopsis thaliana leaf polarity genes REVOLUTA (GRMZM2G469551) and PHABULOSA (GRMZM2G469551) also display specific expression patterns in both emerging leaf primordia and in developing ligules (Supplemental Figures 2B and 3) (Juarez et al, 2004). Two additional transcription factor genes implicated in abaxial patterning of initiating maize leaf primordia (the ARF3 paralogs GRMZM2G030710 and GRMZM2G441325) are likewise upregulated in the preligule region epidermis of maize Figure 3.…”

Genetic modification of plant architecture and variety improvement in rice

“…This mutually antagonistic relationship between KAN and HD-ZIPIII appears to drive lamina growth that is dependent on the activity of the YAB proteins. In maize, two YABBY genes are expressed on the adaxial side of the leaf, suggesting that YABBY genes may direct lateral outgrowth rather than determine cell fate (Juarez et al, 2004b). Consistent with this view, mutations in the rice YABBY gene DROOPING LEAF resulted in defects in midrib formation, possibly owing to reduced cell division (Yamaguchi et al, 2004).…”

A Conserved microRNA Signal Specifies Leaf Polarity

“…HD-ZIPIII proteins contain a START lipid-sterol binding-like domain that is required for protein function (Otsuga et al 2001). Therefore, PHB, PHV, and REV may become activated upon interaction with a ligand, perhaps the meristem-borne signal proposed by the surgical experiments (McConnell et al 2001;Juarez et al 2004a). Such activation could direct the down-regulation of KAN expression, thus suppressing abaxial identity and leading to the specification of adaxial cell fate.…”

“…The adaxial-specific expression of rld1, phb, and potential other hd-zipIII family members is in part mediated by leafbladeless1 (lbl1) (Juarez et al 2004a;M. Juarez and M. Timmermans, unpubl.).…”

“…These latter changes in rld1 expression are associated with an upward curling of the Rld1 leaf blade caused by adaxialization or partial reversal of adaxial/abaxial leaf polarity (Fig. 3c) (Nelson et al 2002;Juarez et al 2004a). The ligule normally forms on the adaxial side of the leaf, and the wild-type adaxial epidermis has distinctive hairs and strengthening cells (Fig.…”