skip to main content

Title: Network analyses identify a transcriptomic proximodistal prepattern in the maize leaf primordium

The formation of developmental boundaries is a common feature of multicellular plants and animals, and impacts the initiation, structure and function of all organs. Maize leaves comprise a proximal sheath that encloses the stem, and a distal photosynthetic blade that projects away from the plant axis. An epidermally derived ligule and a joint‐like auricle develop at the blade/sheath boundary of maize leaves. Mutations disturbing the ligule/auricle region disrupt leaf patterning and impact plant architecture, yet it is unclear how this developmental boundary is established.

Targeted microdissection followed by transcriptomic analyses of young leaf primordia were utilized to construct a co‐expression network associated with development of the blade/sheath boundary.

Evidence is presented for proximodistal gradients of gene expression that establish a prepatterned transcriptomic boundary in young leaf primordia, before the morphological initiation of the blade/sheath boundary in older leaves.

This work presents a conceptual model for spatiotemporal patterning of proximodistal leaf domains, and provides a rich resource of candidate gene interactions for future investigations of the mechanisms of blade/sheath boundary formation in maize.

more » « less
Award ID(s):
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  
Publisher / Repository:
Date Published:
Journal Name:
New Phytologist
Page Range / eLocation ID:
p. 218-227
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Leaf morphogenesis requires growth polarized along three axes—proximal-distal (P-D) axis, medial-lateral axis, and abaxial-adaxial axis. Grass leaves display a prominent P-D polarity consisting of a proximal sheath separated from the distal blade by the auricle and ligule. Although proper specification of the four segments is essential for normal morphology, our knowledge is incomplete regarding the mechanisms that influence P-D specification in monocots such as maize (Zea mays). Here, we report the identification of the gene underlying the semidominant, leaf patterning maize mutant Hairy Sheath Frayed1 (Hsf1). Hsf1 plants produce leaves with outgrowths consisting of proximal segments—sheath, auricle, and ligule—emanating from the distal blade margin. Analysis of three independent Hsf1 alleles revealed gain-of-function missense mutations in the ligand binding domain of the maize cytokinin (CK) receptor Z. mays Histidine Kinase1 (ZmHK1) gene. Biochemical analysis and structural modeling suggest the mutated residues near the CK binding pocket affect CK binding affinity. Treatment of the wild-type seedlings with exogenous CK phenocopied the Hsf1 leaf phenotypes. Results from expression and epistatic analyses indicated the Hsf1 mutant receptor appears to be hypersignaling. Our results demonstrate that hypersignaling of CK in incipient leaf primordia can reprogram developmental patterns in maize.

    more » « less
  2. Summary

    In species with compound leaves, the positions of leaflet primordium initiation are associated with local peaks of auxin accumulation. However, the role of auxin during the late developmental stages and outgrowth of compound leaves remains largely unknown.

    Using genome resequencing approaches, we identified insertion sites at four alleles of theLATERAL LEAFLET SUPPRESSION1(LLS1) gene, encoding the auxin biosynthetic enzyme YUCCA1 inMedicago truncatula.

    Linkage analysis and complementation tests showed that thells1mutant phenotypes were caused by theTnt1insertions that disrupted theLLS1gene. The transcripts ofLLS1can be detected in primordia at early stages of leaf initiation and later in the basal regions of leaflets, and finally in vein tissues at late leaf developmental stages. Vein numbers and auxin content are reduced in thells1‐1mutant. Analysis of thells1 sgl1andlls1 palm1double mutants revealed thatSGL1is epistatic toLLS1, andLLS1works withPALM1in an independent pathway to regulate the growth of lateral leaflets.

    Our work demonstrates that the YUCCA1/YUCCA4 subgroup plays very important roles in the outgrowth of lateral leaflets during compound leaf development ofM. truncatula, in addition to leaf venation.

    more » « less
  3. Hake, Sarah (Ed.)
    The plastochron, the time interval between the formation of two successive leaves, is an important determinant of plant architecture. We genetically and phenotypically investigated many-noded dwarf ( mnd ) mutants in barley. The mnd mutants exhibited a shortened plastochron and a decreased leaf blade length, and resembled previously reported plastochron1 ( pla1 ), pla2 , and pla3 mutants in rice. In addition, the maturation of mnd leaves was accelerated, similar to pla mutants in rice. Several barley mnd alleles were derived from three genes— MND1 , MND4 , and MND8 . Although MND4 coincided with a cytochrome P450 family gene that is a homolog of rice PLA1 , we clarified that MND1 and MND8 encode an N-acetyltransferase-like protein and a MATE transporter-family protein, which are respectively orthologs of rice GW6a and maize BIGE1 and unrelated to PLA2 or PLA3 . Expression analyses of the three MND genes revealed that MND1 and MND4 were expressed in limited regions of the shoot apical meristem and leaf primordia, but MND8 did not exhibit a specific expression pattern around the shoot apex. In addition, the expression levels of the three genes were interdependent among the various mutant backgrounds. Genetic analyses using the double mutants mnd4mnd8 and mnd1mnd8 indicated that MND1 and MND4 regulate the plastochron independently of MND8 , suggesting that the plastochron in barley is controlled by multiple genetic pathways involving MND1 , MND4 , and MND8 . Correlation analysis between leaf number and leaf blade length indicated that both traits exhibited a strong negative association among different genetic backgrounds but not in the same genetic background. We propose that MND genes function in the regulation of the plastochron and leaf growth and revealed conserved and diverse aspects of plastochron regulation via comparative analysis of barley and rice. 
    more » « less
  4. Abstract

    Leaf‐derived signals drive the development of the shoot, eventually leading to flowering. In maize, transcripts of genes that facilitate jasmonic acid (JA) signaling are more abundant in juvenile compared to adult leaf primordia; exogenous application of JA both extends the juvenile phase and delays the decline in miR156 levels. To test the hypothesis that JA promotes juvenility, we measured JA and meJA levels using LC‐MS in successive stages of leaf one development and in later leaves at stages leading up to phase change in both normal maize and phase change mutants. We concurrently measured gibberellic acid (GA), required for the timely transition to the adult phase. Jasmonic acid levels increased from germination through leaf one differentiation, declining in later formed leaves as the shoot approached phase change. In contrast, levels of GA were low in leaf one after germination and increased as the shoot matured to the adult phase. Multiple doses of exogenous JA resulted in the production of as many as three additional juvenile leaves. We analyzed two transcript expression datasets to investigate when gene regulation by miR156 begins in the context of spatiotemporal patterns of JA and GA signaling. Quantifying these hormones in phase change mutants provided insight into how these two hormones control phase‐specific patterns of differentiation. We conclude that the hormone JA is a leaf‐provisioned signal that influences the duration, and possibly the initiation, of the juvenile phase of maize by controlling patterns of differentiation in successive leaf primordia.

    more » « less

    The maize ligule is an epidermis-derived structure that arises from the preligule band (PLB) at a boundary between the blade and sheath. A hinge-like auricle also develops immediately distal to the ligule and contributes to blade angle. Here, we characterize the stages of PLB and early ligule development in terms of topography, cell area, division orientation, cell wall rigidity and auxin response dynamics. Differential thickening of epidermal cells and localized periclinal divisions contributed to the formation of a ridge within the PLB, which ultimately produces the ligule fringe. Patterns in cell wall rigidity were consistent with the subdivision of the PLB into two regions along a distinct line positioned at the nascent ridge. The proximal region produces the ligule, while the distal region contributes to one epidermal face of the auricles. Although the auxin transporter PIN1 accumulated in the PLB, observed differential auxin transcriptional response did not underlie the partitioning of the PLB. Our data demonstrate that two zones with contrasting cellular properties, the preligule and preauricle, are specified within the ligular region before ligule outgrowth.

    more » « less