Genome‐wide transcript analysis of early maize leaf development reveals gene cohorts associated with the differentiation of C₄ Kranz anatomy

Abstract

Summary Photosynthesis underpins the viability of most ecosystems, with C4 plants that exhibit ‘Kranz’ anatomy being the most efficient primary producers. Kranz anatomy is characterized by closely spaced veins that are encircled by two morphologically distinct photosynthetic cell types. Although Kranz anatomy evolved multiple times, the underlying genetic mechanisms remain largely elusive, with only the maize scarecrow gene so far implicated in Kranz patterning. To provide a broader insight into the regulation of Kranz differentiation, we performed a genome‐wide comparative analysis of developmental trajectories in Kranz (foliar leaf blade) and non‐Kranz (husk leaf sheath) leaves of the C4 plant maize. Using profile classification of gene expression in early leaf primordia, we identified cohorts of genes associated with procambium initiation and vascular patterning. In addition, we used supervised classification criteria inferred from anatomical and developmental analyses of five developmental stages to identify candidate regulators of cell‐type specification. Our analysis supports the suggestion that Kranz anatomy is patterned, at least in part, by a SCARECROW/SHORTROOT regulatory network, and suggests likely components of that network. Furthermore, the data imply a role for additional pathways in the development of Kranz leaves.

Combined Large-Scale Phenotyping and Transcriptomics in Maize Reveals a Robust Growth Regulatory Network

“…Although analyses of transcriptional variation during maize leaf development have provided us with new insights, all these studies were restricted to one genetic background (Li et al, 2010;Pick et al, 2011;Liu et al, 2013b;Wang et al, 2013Wang et al, , 2014Yu et al, 2015). Adding an additional layer of information, phenotypic variation in mapping populations, and combining this with transcriptome variation in these populations offers new opportunities to identify genes and regulatory mechanisms that are at the basis of phenotypic differences (Andorf et al, 2012).…”

“…Transcriptional dynamics during early development of embryonic leaves were surveyed by Liu et al (2013b) and Yu et al (2015). Additionally, the regulatory and functional differentiation of various leaf cell types was examined by transcriptome analysis (Li et al, 2010;Wang et al, 2013Wang et al, , 2014. The transcriptional variation between tissue types and cell types during development (Li et al, 2010;Wang et al, 2013Wang et al, , 2014 illustrates the importance of focusing the analysis of a given process on those tissues where the process takes place.…”

“…Additionally, the regulatory and functional differentiation of various leaf cell types was examined by transcriptome analysis (Li et al, 2010;Wang et al, 2013Wang et al, , 2014. The transcriptional variation between tissue types and cell types during development (Li et al, 2010;Wang et al, 2013Wang et al, , 2014 illustrates the importance of focusing the analysis of a given process on those tissues where the process takes place. Since leaf growth is driven by proliferation and expansion, zooming in on proliferative and/or expanding tissue is required to identify the regulatory networks underlying leaf development.…”

Transcriptome dynamics of developing maize leaves and genomewide prediction ofciselements and their cognate transcription factors

“…This set of data provided a global picture of the transcriptional dynamics of genes for early leaf development during maize seed germination and shed light on the succession of biological processes during this period. Wang et al (7) investigated the transcriptomes of Kranz (i.e., the foliar leaf blade) and non-Kranz (the husk leaf sheath) maize leaves to identify cohorts of genes associated with procambium initiation and vascular patterning. Recently, Wang et al (8) conducted comparative transcriptomic and metabolomic analyses of developing leaves in maize and rice and identified putative structural and regulatory components important for C4 and C3 photosynthesis.…”

Comparative genomics and trait evolution in Cleomaceae, a model family for ancient polyploidy

“…Recent work has shown that the SCARECROW (SCR) gene that is responsible for vein formation in roots, can produce proliferated bundle sheath cells as well as other changes that can be coupled to the shift to the Kranz anatomy (Slewinski et al, 2012). Further work supports this relation by describing the role that the upstream interacting partner of SCR, SHORT-ROOT (SHR) plays in the variations in anatomy seen in various C4 species (Wang et al, 2013;Slewinski et al, 2014).…”