Organogenetic capacity of leaves: The significance of marginal blastozones in angiosperms

Hagemann, Wolfgang; Gleissberg, Stefan

doi:10.1007/bf00984901

Cited by 185 publications

(191 citation statements)

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“…Similar observations were reported from the Lanceolate mutant (33) and from transgenic plants expressing a TKn2-SRDX construct under the control of the FIL promoter (8). In tomato, leaflets initiate from ridges of meristematic cells at the leaf margin called the marginal blastozone (7). In tf mutants, the marginal blastozone is narrower than in WT including fewer cells with large intercellular spaces ( Fig.…”

Section: Discussionsupporting

confidence: 70%

“…At this developmental stage, leaf primordia initiate lateral leaflets on their margins. Because tf mutants displayed a defect in lateral leaflet initiation resulting in the constant trifoliate leaf pattern, we hypothesized a histological defect during development of the marginal blastozone, the organogenetic competent region of the leaf margin (7). To investigate this, we analyzed transverse sections of the leaf rachis of WT and tf-2 plants ( Table S1).…”

Section: Resultsmentioning

confidence: 99%

“…However, in many compound leaved species, such as tomato or Cardamine hirsuta, KNOXI expression is reactivated during leaf development (5,6). Early leaf development proceeds through three stages: initiation, primary morphogenesis (PM), and secondary morphogenesis (SM), with leaflets being initiated at the PM stage (7). In tomato, KNOXI (e.g., LeT6/TKn2) activity is specifically required at the PM stage, where it inhibits differentiation (8).…”

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confidence: 99%

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Trifoliate encodes an MYB transcription factor that modulates leaf and shoot architecture in tomato

Naz

Raman

Martinez

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Leaf morphology and the pattern of shoot branching determine to a large extent the growth habit of seed plants. Until recently, the developmental processes that led to the establishment of these morphological structures seemed unrelated. Here, we show that the tomato Trifoliate ( Tf ) gene plays a crucial role in both processes, affecting the formation of leaflets in the compound tomato leaf and the initiation of axillary meristems in the leaf axil. Tf encodes a myeloblastosis oncoprotein (MYB)-like transcription factor related to the Arabidopsis thaliana LATERAL ORGAN FUSION1 (LOF1) and LOF2 proteins. Tf is expressed in the leaf margin, where leaflets are formed, and in the leaf axil, where axillary meristems initiate. During tomato ontogeny, expression of Tf in young leaf primordia increases, correlating with a rise in leaf dissection (heteroblasty). Formation of leaflets and initiation of axillary meristems can be traced back to groups of pluripotent cells. Tf function is required to inhibit differentiation of these cells and thereby to maintain their morphogenetic competence, a fundamental process in plant development. KNOTTED1-LIKE proteins, which are known regulators in tomato leaf dissection, require Tf activity to exert their function in the basal part of the leaf. Similarly, the plant hormone auxin needs Tf activity to initiate the formation of lateral leaflets. Thus, leaf dissection and shoot branching rely on a conserved mechanism that regulates the morphogenetic competence of cells at the leaf margin and in the leaf axil.

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Section: Discussionsupporting

confidence: 70%

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

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Trifoliate encodes an MYB transcription factor that modulates leaf and shoot architecture in tomato

Naz

Raman

Martinez

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…Leaf dissection and differentiation gradients-Marginal areas with the competence for primordium formation (marginal blastozones) are characterized by the absence of histological differentiation marked by cell vacuolation or presence of idioblasts (Hagemann and Gleissberg, 1996). The onset of tissue differentiation at the margin may disable further primordium formation.…”

Section: Discussionmentioning

confidence: 99%

“…This process may determine whether or not lateral primordia are initiated during intercalary elongation of the petiole, conditioning different architectures of the mature leaf (Gleissberg, 2002). Blastozone inactivation or loss is frequently accompanied by cell vacuolation and trichome formation, indicating that the organogenic ability of blastozones precludes histogenic processes and requires densely cytoplasmic meristematic tissue (Hagemann and Gleissberg, 1996). Progressing histogenesis may therefore restrict blastozones and affect patterns of organogenic activity within the leaf.…”

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confidence: 99%

Comparative analysis of leaf shape development in Eschscholzia californica and other Papaveraceae‐Eschscholzioideae

Gleissberg

2004

American J of Botany

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Dissected leaves in Papaveraceae-Eschscholzioideae have an architecture frequently encountered in the basal eudicot clade Ranunculales that could represent an ancestral condition for eudicots. Developmental morphology of foliage leaves was investigated using scanning electron microscopy and focusing on primordium formation activity (primary morphogenesis) at the leaf margin. Eschscholzia californica, E. lobii, and Hunnemannia fumariaefolia had a polyternate-acropetal mode of leaf dissection. Segment formation continued around the whole leaf blade periphery. Differences in mature leaf architecture was traced to variations in regional blastozone activity and duration. Epidermal cell size measurements in E. californica indicated that the leaf tip tissue starts to differentiate already at the onset of organogenic activity and that tip cells remain larger than epidermal cells at the basal margins during further growth. It is argued that early differentiation of the tip does not set up a general basipetal differentiation gradient, but is a local effect that allows acropetal pinna initiation to occur in subapical blastozones. In Dendromecon, secondarily entire leaves have evolved through the loss of primordium formation activity. Marginal corrugations found in Dendromecon form late in development and are not reminiscent of lateral primordia.Key words: blastozone; Dendromecon; Eschscholzia; histogenesis; Hunnemannia; leaf dissection; primary morphogenesis.The wide variation in number and arrangement of pinnae and other leaf segments such as lobes and serrations in many dicot plants arises during an early organogenic phase of leaf development before leaves have grown to a size of 1 or 2 mm. The formation of marginal primordia during this critical period of primary morphogenesis proceeds in often distinct directions, such as acropetal or basipetal. Certain parts of the leaf blastozone (the marginal regions competent for primordium formation), such as along the developing petiole and rachis units, may become permanently inactivated at an early stage. This process may determine whether or not lateral primordia are initiated during intercalary elongation of the petiole, conditioning different architectures of the mature leaf (Gleissberg, 2002). Blastozone inactivation or loss is frequently accompanied by cell vacuolation and trichome formation, indicating that the organogenic ability of blastozones precludes histogenic processes and requires densely cytoplasmic meristematic tissue (Hagemann and Gleissberg, 1996). Progressing histogenesis may therefore restrict blastozones and affect patterns of organogenic activity within the leaf.Beside region-specific blastozone inactivation via marginal histogenesis, a major determinant of dissection patterns may be different rates of primordium formation within the blastozone. Species with multi-dissected leaves often have periplastic blastozones, in which primordium formation activity continues around the entire growing periphery. Here, directional initiation of pinnae is soon accompani...

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Genetic Control of Leaf Shape

Martinez

Sinha

2013

Encyclopedia of Life Sciences

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The variability in leaf morphology is vast; therefore, an understanding of how leaves achieve this diversity has captured the attention of many developmental biologists. Genetic mechanisms that regulate leaf shape are repeated throughout both development and between species. Leaves initiate off the shoot apical meristem and development proceeds from cell division to cell elongation. Leaf initiation and the establishment of the three main axes of a leaf are largely directed by the plant hormone auxin. Work across species reveals that adjustments to the repeated interaction of auxin, gene expression changes and small ribonucleic acid (RNA) regulation allowed species‐specific leaf shape differences to emerge. Further, genetic interactions leading to patterning in simple leaf development are reiterated during establishment of leaf complexity. To understand leaf development in an evolutionary context, future research must take advantage of the ever‐expanding genomic tools in nonmodel organisms that exhibit leaf shape diversity. Key Concepts: Leaves originate from clusters of stem cells called meristems. The development of leaves occurs along three main axes: (1) adaxial/abaxial, (2) proximal/distal and (3) medial/lateral. The development of both meristems and leaves involve morphogenetic activity in zones which are defined by distinct gene expression and cell division/elongation patterns. The transport and concentration of the hormone auxin largely directs many aspects of leaf morphogenesis. Leaf and leaflet initiation first begin with the formation of auxin maxima. Recycling of genetic mechanisms is a theme that occurs throughout leaf development.

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Organogenetic capacity of leaves: The significance of marginal blastozones in angiosperms

Cited by 185 publications

References 32 publications

Trifoliate encodes an MYB transcription factor that modulates leaf and shoot architecture in tomato

Trifoliate encodes an MYB transcription factor that modulates leaf and shoot architecture in tomato

Comparative analysis of leaf shape development in Eschscholzia californica and other Papaveraceae‐Eschscholzioideae

Genetic Control of Leaf Shape

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