Unraveling the KNOTTED1 regulatory network in maize meristems

Abstract

KNOTTED1 (KN1)-like homeobox (KNOX) transcription factors function in plant meristems, self-renewing structures consisting of stem cells and their immediate daughters. We defined the KN1 cistrome in maize inflorescences and found that KN1 binds to several thousand loci, including 643 genes that are modulated in one or multiple tissues. These KN1 direct targets are strongly enriched for transcription factors (including other homeobox genes) and genes participating in hormonal pathways, most significantly auxin, demonstrating that KN1 plays a key role in orchestrating the upper levels of a hierarchical gene regulatory network that impacts plant meristem identity and function.

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

“…Dominant Lg3 mutants are characterized by leaf patterning defects that include displacement of the ligule over the midrib or deletion of the ligule (Fowler and Freeling, 1996;Muehlbauer et al, 1997Muehlbauer et al, , 1999. lg3 is bound by KN1 and RNAseq data show that lg3 is highly upregulated in Kn1-N leaves (Bolduc et al, 2012b). We found that lg3 transcript is significantly higher in preligule tissue than in blade tissue and is also higher in preligule than in sheath tissue, although this latter difference was not statistically significant ( Figure 4G).…”

“…Given that KNOX-BEL-auxin modules act in multiple contexts during plant development, it is possible that different SBP family members are expressed depending on context, thus contributing to the elaboration of different developmental boundaries. Intriguingly, two auxin transport genes, Zm-PIN1a and So-PIN1, are upregulated in preligule epidermal cells and are also bound by KN1 and upregulated in Kn1-N mutant leaves (Bolduc et al, 2012b). This finding suggests that KN1 directly activates Zm-PIN1a and SoPIN1 transcription at ectopic boundaries and suggests a model in which auxin transport by PIN proteins is activated at the KNOX presence/absence boundary at the base of wild-type leaf primordia.…”

“…Our data show that maize bel12 (GRMZM2G154641) is significantly upregulated in the preligule region, whereas bel14 (GRMZM2G125976) is expressed at low levels in the blade, moderate levels in the sheath, and most highly in the ligule region ( Figure 4G; Supplemental Table 4). Both bel12 and bel14 are bound by KN1 and are upregulated in Kn1-N/Kn1-N leaves compared with the wild type, although the difference is not statistically significant in the case of bel14 (Bolduc et al, 2012b).…”

“…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). In Arabidopsis, BEL1-like homeodomain (BELL) proteins form heterodimers with KNOX proteins in combinations that determine target selection and subcellular localization (Bellaoui Smith et al, 2002;Bhatt et al, 2004;Hackbusch et al, 2005;Cole et al, 2006).…”

RiceLHS1/OsMADS1Controls Floret Meristem Specification by Coordinated Regulation of Transcription Factors and Hormone Signaling Pathways

“…Interactions between cytokinin signaling and homeodomain transcription factors govern meristem maintenance in Arabidopsis, maize, and rice (Gordon et al, 2009;Tsuda et al, 2011;Bolduc et al, 2012). In OsMADS1 knockdown panicles, we detected an overall increased activity of cytokinin pathway genes, examples being LONELY GUY (LOG) family members, a predicted receptor, HKL1/CRL4, and several response regulator (RR) genes (Supplemental Table S4).…”