Overexpression of <i>KNAT1</i> in Lettuce Shifts Leaf Determinate Growth to a Shoot-Like Indeterminate Growth Associated with an Accumulation of Isopentenyl-Type Cytokinins

Frugis, Giovanna; Giannino, Donato; Mele, Giovanni; Nicolodi, Chiara; Chiappetta, Adriana; Bitonti, Maria Beatrice; Innocenti, A. M.; Dewitte, Walter; Onckelen, Harry Van; Mariotti, D.

doi:10.1104/pp.126.4.1370

Cited by 118 publications

(85 citation statements)

References 29 publications

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“…First, the lobed leaf phenotype is reminiscent of plants that overproduce cytokinins (Estruch et al, 1993). Likewise, the higher rate of regeneration observed in DEX-induced KNAT2-GR explants is a typical cytokinin feature that was also observed in transgenic lettuce that overexpressed KNAT1 (Frugis et al, 1999(Frugis et al, , 2001. Third, the KNAT2-GR plants grown in the presence DEX exhibited an inhibition of hypocotyl elongation and epinastic cotyledons, much like the KNAT2-GR plant grown in the presence of BAP (Cary et al, 1995;personal observations).…”

Section: Discussionmentioning

confidence: 84%

“…Third, the KNAT2-GR plants grown in the presence DEX exhibited an inhibition of hypocotyl elongation and epinastic cotyledons, much like the KNAT2-GR plant grown in the presence of BAP (Cary et al, 1995;personal observations). Fourth, the KNAT2-GR activation led to a delay in leaf senescence, a phenotype induced by both cytokinins and overexpression of KN1 in tobacco and KNAT1 in lettuce (Gan and Amasino, 1995;Ori et al, 1999;Frugis et al, 2001). Finally, preliminary differential screening indicated common targets between cytokinin and KNAT2 (O. Hamant, F. Nogré, J. Traas, and V. Pautot, unpublished data).…”

Section: Discussionmentioning

confidence: 99%

“…In particular, the relation with cytokinins has been quite well documented. For example, overexpression of the maize (Zea mays) KNOTTED 1 gene KN1, the rice (Oryza sativa) KNOX gene OSH1, the tobacco (Nicotiana tabacum) KNOX gene NTH15, and the Arabidopsis KNAT1 gene in lettuce (Lactuca sativa) leads to higher cytokinin levels (Tamaoki et al, 1997;Kusaba et al, 1998a;Hewelt et al, 2000;Frugis et al, 2001). Conversely, plants overproducing cytokinins exhibit higher levels of KNAT1 and STM mRNA (Rupp et al, 1999).…”

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confidence: 99%

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The KNAT2 Homeodomain Protein Interacts with Ethylene and Cytokinin Signaling

Hamant¹,

Nogué

Belles‐Boix³

et al. 2002

Plant Physiology

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Using a transgenic line that overexpresses a fusion of the KNAT2 (KNOTTED-like Arabidopsis) homeodomain protein and the hormone-binding domain of the glucocorticoid receptor (GR), we have investigated the possible relations between KNAT2 and various hormones. Upon activation of the KNAT2-GR fusion, we observed a delayed senescence of the leaves and a higher rate of shoot initiation, two processes that are also induced by cytokinins and inhibited by ethylene. Furthermore, the activation of the KNAT2-GR fusion induced lobing of the leaves. This feature was partially suppressed by treatment with the ethylene precursor 1-aminocyclopropane-1-carboxylic acid, or by the constitutive ethylene response ctr1 mutation. Conversely, some phenotypic traits of the ctr1 mutant were suppressed by the activation of the KNAT2-GR fusion. These data suggest that KNAT2 acts synergistically with cytokinins and antagonistically with ethylene. In the shoot apical meristem, the KNAT2 gene is expressed in the L3 layer and the rib zone. 1-Aminocyclopropane-1-carboxylic acid treatment restricted the KNAT2 expression domain in the shoot apical meristem and reduced the number of cells in the L3. The latter effect was suppressed by the activation of the KNAT2-GR construct. Conversely, the KNAT2 gene expression domain was enlarged in the ethylene-resistant etr1-1 mutant or in response to cytokinin treatment. These data suggest that ethylene and cytokinins act antagonistically in the meristem via KNAT2 to regulate the meristem activity.Plant organs are formed continuously during postembryonic development from groups of indeterminate meristematic cells. In Angiosperms like Arabidopsis, the cells within the shoot apical meristem (SAM) are distributed in three layers: L1, L2, and L3 (Clark, 1997; Barton, 1998). The cells derived from the L1 will preferentially form the epidermis, whereas L2 and L3 layers will give rise to the inner parts of the organs. The SAM is furthermore organized in three distinct zones: the peripheral zone, the central zone, and the rib zone. The central zone maintains a population of founder cells. Cells are recruited to the peripheral zone and the rib zone from the central zone, and generate the lateral organs and the inner parts of the stem, respectively. The family of KNOX (KNOTTED homeobox) genes plays a crucial role in the SAM: in Arabidopsis, the KNAT (KNOTTED-like in Arabidopsis) family comprises eight members (Serikawa et al., 1996;Reiser et al., 2000;Semiarti et al., 2001). Of these, four have been associated with meristem function. The best characterized is the STM (SHOOTMERISTEMLESS) gene, which is absolutely required for meristem maintenance (Long et al., 1996). More recently, loss-of-function mutants have been described for KNAT1 (Douglas et al., 2002;Venglat et al., 2002). The molecular characterization of the bp (brevipedicellus) mutant of Arabidopsis has revealed that BP encodes the KNAT1 protein. In addition to its role in meristem maintenance in redundancy with STM, BP plays a key role in regulating the inf...

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Section: Discussionmentioning

confidence: 84%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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The KNAT2 Homeodomain Protein Interacts with Ethylene and Cytokinin Signaling

Hamant¹,

Nogué

Belles‐Boix³

et al. 2002

Plant Physiology

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“…Ectopic expression of KNOX genes induces speciesspeciWc alterations in leaf shape and morphology, as well as ectopic meristem/shoot production. Many of these phenotypes are similar to transgenics expressing bacterial ipt genes, and indeed ectopic KNOX expression alters not only cytokinin, but also gibberellin and auxin metabolism (Tamaoki et al 1997;Hewelt et al 2000;Frugis et al 2001;Sakamoto et al 2001). In tobacco, mild KNOX misexpression phenotypes that are similar to BBM misexpression phenotypes include adventitious shoot formation, rumpled leaves with a disorganized or absent palisade parenchyma layer and Xowers that are pale to white in colour and that have stamens that are shorter than those from wild-type plants ( Kano-Murakami et al 1993;Sinha et al 1993;Tamaoki et al 1997;Sato et al 1998;Postma-Haarsma et al 1999).…”

Section: Discussionmentioning

confidence: 92%

Heterologous expression of the BABY BOOM AP2/ERF transcription factor enhances the regeneration capacity of tobacco (Nicotiana tabacum L.)

Srinivasan

Liu

Heidmann

et al. 2006

Planta

134

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Gain-of-function studies have shown that ectopic expression of the BABY BOOM (BBM) AP2/ ERF domain transcription factor is suYcient to induce spontaneous somatic embryogenesis in Arabidopsis (Arabidopsis thaliana (L.) Heynh) and Brassica napus (B. napus L.) seedlings. Here we examined the eVect of ectopic BBM expression on the development and regenerative capacity of tobacco (Nicotiana tabacum L.) through heterologous expression of Arabidopsis and B. napus BBM genes. 35S::BBM tobacco lines exhibited a number of the phenotypes previously observed in 35S::BBM Arabidopsis and B. napus transgenics, including callus formation, leaf rumpling, and sterility, but they did not undergo spontaneous somatic embryogenesis. 35S::BBM plants with severe ectopic expression phenotypes could not be assessed for enhanced regeneration at the seedling stage due to complete male and female sterility of the primary transformants, therefore fertile BBM ectopic expression lines with strong misexpression phenotypes were generated by expressing a steroid-inducible, posttranslationally controlled BBM fusion protein (BBM:GR) under the control of a 35S promoter. These lines exhibited spontaneous shoot and root formation, while somatic embryogenesis could be induced from in-vitro germinated seedling hypocotyls cultured on media supplemented with cytokinin. Together these results suggest that ectopic BBM expression in transgenic tobacco also activates cell proliferation pathways, but diVerences exist between Arabidopsis/B. napus and N. tabacum with respect to their competence to respond to the BBM signalling molecule.

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“…A role for cytokinins in the SAM also was indicated by the expression of AtCKX1 and AtCKX2, which are members of the two different AtCKX classes, in the shoot apex ( Figures 11A and 11E). A possibly mutual interaction of cytokinins and homeobox genes of the SAM has been reported (Sinha et al, 1993;Ori et al, 1999;Rupp et al, 1999;Frugis et al, 2001). These could present elements of a regulatory pathway that quantitatively control meristem activity.…”

Section: Cytokinin Is a Positive Regulator Of Shoot Meristem Activitymentioning

confidence: 99%

Cytokinin-Deficient Transgenic Arabidopsis Plants Show Multiple Developmental Alterations Indicating Opposite Functions of Cytokinins in the Regulation of Shoot and Root Meristem Activity

Werner

Motyka

Laucou³

et al. 2003

Plant Cell

Self Cite

1,272

1,243

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Cytokinins are hormones that regulate cell division and development. As a result of a lack of specific mutants and biochemical tools, it has not been possible to study the consequences of cytokinin deficiency. Cytokinin-deficient plants are expected to yield information about processes in which cytokinins are limiting and that, therefore, they might regulate. We have engineered transgenic Arabidopsis plants that overexpress individually six different members of the cytokinin oxidase/dehydrogenase ( AtCKX ) gene family and have undertaken a detailed phenotypic analysis. Transgenic plants had increased cytokinin breakdown (30 to 45% of wild-type cytokinin content) and reduced expression of the cytokinin reporter gene ARR5 : GUS ( ␤ -glucuronidase). Cytokinin deficiency resulted in diminished activity of the vegetative and floral shoot apical meristems and leaf primordia, indicating an absolute requirement for the hormone. By contrast, cytokinins are negative regulators of root growth and lateral root formation. We show that the increased growth of the primary root is linked to an enhanced meristematic cell number, suggesting that cytokinins control the exit of cells from the root meristem. Different AtCKX-green fluorescent protein fusion proteins were localized to the vacuoles or the endoplasmic reticulum and possibly to the extracellular space, indicating that subcellular compartmentation plays an important role in cytokinin biology. Analyses of promoter: GUS fusion genes showed differential expression of AtCKX genes during plant development, the activity being confined predominantly to zones of active growth. Our results are consistent with the hypothesis that cytokinins have central, but opposite, regulatory functions in root and shoot meristems and indicate that a fine-tuned control of catabolism plays an important role in ensuring the proper regulation of cytokinin functions.

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Overexpression of KNAT1 in Lettuce Shifts Leaf Determinate Growth to a Shoot-Like Indeterminate Growth Associated with an Accumulation of Isopentenyl-Type Cytokinins

Cited by 118 publications

References 29 publications

The KNAT2 Homeodomain Protein Interacts with Ethylene and Cytokinin Signaling

The KNAT2 Homeodomain Protein Interacts with Ethylene and Cytokinin Signaling

Heterologous expression of the BABY BOOM AP2/ERF transcription factor enhances the regeneration capacity of tobacco (Nicotiana tabacum L.)

Cytokinin-Deficient Transgenic Arabidopsis Plants Show Multiple Developmental Alterations Indicating Opposite Functions of Cytokinins in the Regulation of Shoot and Root Meristem Activity

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