How to Pattern a Leaf

Abstract

Leaf development presents a tremendous resource for tackling the question of patterning in biology. Leaves can be simple or highly dissected. They may have elaborated parts such as the tendrils of a pea leaf or the rolled blade of a carnivorous pitcher plant. Despite the variation in size, shape, and function, all leaves initiate in the same manner: from the flanks of a meristem. The maize leaf is useful for analysis of patterning due to the wealth of mutants and the distinct tissues along the proximal distal axis. The blade is distal, the sheath is proximal, and the ligule forms at the blade/sheath boundary. Establishment of this boundary involves the transcription factors LIGULELESS1 and LIGULELESS2 and the kinase LIGULELESS NARROW. The meristem-specific protein KNOTTED1 (KN1) binds and modulates the lg2 gene. Given the localization of KN1 at the proximal end of the leaf from the time of inception, we hypothesize that KN1 has a role in establishing the very proximal end of the leaf, whereas an auxin maximum guides the growing distal tip.

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

“…Dominant maize mutants that ectopically express knox genes displace proximal sheath tissue into the distal blade, whereas mutants that are defective in auxin transport exhibit ectopic accumulation of KNOX proteins and similar proximaldistal leaf patterning defects (Freeling and Hake, 1985;Sinha and Hake, 1990;Fowler and Freeling, 1996;Foster et al, 1999;Tsiantis et al, 1999;Scanlon et al, 2002;Ramirez et al, 2009). These observations support a model whereby KNOX accumulation specifies the proximal sheath compartment of very young primordia, and auxin restricts KNOX protein accumulation from distal leaf domains (Bolduc et al, 2012a). Such antagonism between auxin and KNOX is a module that acts in multiple contexts during plant development (Scanlon, 2003;Gallavotti et al, 2008;Hay and Tsiantis, 2010).…”

“…Localization of PIN-mediated auxin transport at the P0 correlates with subsequent knox gene downregulation ( Figure 7E) . At P1 and later, KNOX accumulates at the base of the primordium ( Figures 7F and 7G), while the distal portion of the primordium becomes an auxin source (Jackson, 2002;Bolduc et al, 2012a). Our data show that the preblade region is enriched for auxin-related transcripts, whereas the preligule and presheath regions are enriched for homeobox transcription factors.…”

“…These observations form the basis of a model in which KNOX specifies the presheath domain during early leaf development (Bolduc et al, 2012a). Given the proposed role of KNOX in leaf proximal-distal patterning, we investigated genes that are DE in our data and are also bound and modulated by KN1 protein (Bolduc et al, 2012b).…”

“…knotted1-like homeobox (knox) genes encode transcription factors that function in meristem maintenance and leaf initiation. knotted1 (kn1) transcripts accumulate at high levels in the maize SAM but are restricted from incipient and emerging leaf primordia where auxin levels are high (Jackson et al, 1994;Bolduc et al, 2012a;O'Connor et al, 2014). Dominant maize mutants that ectopically express knox genes displace proximal sheath tissue into the distal blade, whereas mutants that are defective in auxin transport exhibit ectopic accumulation of KNOX proteins and similar proximaldistal leaf patterning defects (Freeling and Hake, 1985;Sinha and Hake, 1990;Fowler and Freeling, 1996;Foster et al, 1999;Tsiantis et al, 1999;Scanlon et al, 2002;Ramirez et al, 2009).…”

The Barley Uniculme4 Gene Encodes a BLADE-ON-PETIOLE-Like Protein That Controls Tillering and Leaf Patterning

“…Gene expression in the developing ligule is consistent with a specific role for Cul4 in the differentiation of this structure. Other genes required for ligule development have been identified from genetic analyses in maize (Zea mays; Bolduc et al, 2012). Among them, LIGULELESS2 (LG2) encodes a TGA basic Leu zipper transcription factor (Walsh et al, 1998), which was proposed to link proximal-distal leaf patterning signals and the induction of ligule development (Bolduc et al, 2012).…”