Genetic evidence that the endodermis is essential for shoot gravitropism in <i>Arabidopsis thaliana</i>

Fukaki, Hidehiro; Wysocka‐Diller, Joanna; Kato, Tadahiro; Fujisawa, Hisao; Benfey, Philip N.; Tasaka, Masao

doi:10.1046/j.1365-313x.1998.00137.x

Cited by 347 publications

(286 citation statements)

References 29 publications

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“…As in roots, the SHR pathway regulates radial patterning around vascular tissue in the hypocotyl of Arabidopsis (Fukaki et al, 1998;Tasaka et al, 1999), but roles in shoot development have not been well described in monocots, with the only functional insight provided by the Zmshr1 loss-of-function mutant in maize, in which vascular patterning in the leaf is perturbed (Slewinski et al, 2014). Vascular perturbations in Zmshr1 plants are subtle, however, as might be expected given the potential for redundancy with ZmSHR2 and ZmSHR2h.…”

Section: Discussionmentioning

confidence: 99%

SHORTROOT-Mediated Increase in Stomatal Density Has No Impact on Photosynthetic Efficiency

et al. 2017

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ORCID IDs: 0000-0003-4287-6927 (M.L.S.); 0000-0002-7609-0378 (O.V.S.); 0000-0001-5932-6468 (B.J.W.); 0000-0002-4621-1490 (P.W.); 0000-0001-7648-3924 (J.A.L.).The coordinated positioning of veins, mesophyll cells, and stomata across a leaf is crucial for efficient gas exchange and transpiration and, therefore, for overall function. In monocot leaves, stomatal cell files are positioned at the flanks of underlying longitudinal leaf veins, rather than directly above or below. This pattern suggests either that stomatal formation is inhibited in epidermal cells directly in contact with the vein or that specification is induced in cell files beyond the vein. The SHORTROOT pathway specifies distinct cell types around the vasculature in subepidermal layers of both root and shoots, with cell type identity determined by distance from the vein. To test whether the pathway has the potential to similarly pattern epidermal cell types, we expanded the expression domain of the rice (Oryza sativa ssp japonica) OsSHR2 gene, which we show is restricted to developing leaf veins, to include bundle sheath cells encircling the vein. In transgenic lines, which were generated using the orthologous ZmSHR1 gene to avoid potential silencing of OsSHR2, stomatal cell files were observed both in the normal position and in more distant positions from the vein. Contrary to theoretical predictions, and to phenotypes observed in eudicot leaves, the increase in stomatal density did not enhance photosynthetic capacity or increase mesophyll cell density. Collectively, these results suggest that the SHORTROOT pathway may coordinate the positioning of veins and stomata in monocot leaves and that distinct mechanisms may operate in monocot and eudicot leaves to coordinate stomatal patterning with the development of underlying mesophyll cells.The coordinated differentiation of cell types within an organ is a crucial component of morphogenesis, necessary to ensure that the final form is appropriate for function. In this regard, photosynthetic function in plant leaves requires that chloroplast-containing cells in the middle leaf layers are interspersed with veins (to supply water and to redistribute metabolites) and are overlaid with stomatal pores through which carbon dioxide can enter the leaf. In grass leaves, cellular arrangements are defined by parallel longitudinal veins that extend from the base of the leaf sheath to the tip of the leaf blade, with short transverse veins interconnecting the longitudinal network (Sharman, 1942;Esau, 1943;Nelson and Dengler, 1997). This vascular framework underpins linear files of stomata in the epidermis, with each vein being flanked by one to three rows of stomata on both the medial and lateral sides (Stebbins and Shah, 1960). The genetic mechanisms that ensure optimal photosynthetic capacity in grass leaves, by coordinating the development of veins, photosynthetic cell types, and stomata, are not known.Grass leaves develop basipetally such that cellular differentiation proceeds from the tip of the leaf to the base, ...

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Section: Discussionmentioning

confidence: 99%

SHORTROOT-Mediated Increase in Stomatal Density Has No Impact on Photosynthetic Efficiency

et al. 2017

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“…Mutants and transgenic lines used in this study are as follows: jkd-4 (Columbia-0 [Col-0]) and mgp-i as described by Welch et al (2007); scr-3 as described by Fukaki et al (1996); scr-4 (Wassilewskija) as described by Fukaki et al (1998); shr-2 as described by Nakajima et al (2001).…”

Section: Plant Growth and Transformationmentioning

confidence: 99%

Arabidopsis BIRD Zinc Finger Proteins Jointly Stabilize Tissue Boundaries by Confining the Cell Fate Regulator SHORT-ROOT and Contributing to Fate Specification

et al. 2015

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Plant cells cannot rearrange their positions; therefore, sharp tissue boundaries must be accurately programmed. Movement of the cell fate regulator SHORT-ROOT from the stele to the ground tissue has been associated with transferring positional information across tissue boundaries. The zinc finger BIRD protein JACKDAW has been shown to constrain SHORT-ROOT movement to a single layer, and other BIRD family proteins were postulated to counteract JACKDAW's role in restricting SHORT-ROOT action range. Here, we report that regulation of SHORT-ROOT movement requires additional BIRD proteins whose action is critical for the establishment and maintenance of the boundary between stele and ground tissue. We show that BIRD proteins act in concert and not in opposition. The exploitation of asymmetric redundancies allows the separation of two BIRD functions: constraining SHORT-ROOT spread through nuclear retention and transcriptional regulation of key downstream SHORT-ROOT targets, including SCARECROW and CYCLIND6. Our data indicate that BIRD proteins promote formative divisions and tissue specification in the Arabidopsis thaliana root meristem ground tissue by tethering and regulating transcriptional competence of SHORT-ROOT complexes. As a result, a tissue boundary is not "locked in" after initial patterning like in many animal systems, but possesses considerable developmental plasticity due to continuous reliance on mobile transcription factors.

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“…8). These differences are unlikely to reflect that SHR is essential for radial patterning only in root-derived organs, since this gene product is also required for the formation of the starch-sheath layer in shoot tissues (Fukaki et al, 1998). Instead, it is most likely that another GRAS family member (Pysh et al, 1999) performs a SHR-like patterning function in this tissue.…”

Section: Shr Is Not Required For Correct Patterning Of Anchor Root Timentioning

confidence: 99%

SHORT-ROOT Regulates Primary, Lateral, and Adventitious Root Development in Arabidopsis

et al. 2010

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SHORT-ROOT (SHR) is a well-characterized regulator of radial patterning and indeterminacy of the Arabidopsis (Arabidopsis thaliana) primary root. However, its role during the elaboration of root system architecture remains unclear. We report that the indeterminate wild-type Arabidopsis root system was transformed into a determinate root system in the shr mutant when growing in soil or agar. The root growth behavior of the shr mutant results from its primary root apical meristem failing to initiate cell division following germination. The inability of shr to reactivate mitotic activity in the root apical meristem is associated with the progressive reduction in the abundance of auxin efflux carriers, PIN-FORMED1 (PIN1), PIN2, PIN3, PIN4, and PIN7. The loss of primary root growth in shr is compensated by the activation of anchor root primordia, whose tissues are radially patterned like the wild type. However, SHR function is not restricted to the primary root but is also required for the initiation and patterning of lateral root primordia. In addition, SHR is necessary to maintain the indeterminate growth of lateral and anchor roots. We conclude that SHR regulates a wide array of Arabidopsis root-related developmental processes.

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Genetic evidence that the endodermis is essential for shoot gravitropism in Arabidopsis thaliana

Cited by 347 publications

References 29 publications

SHORTROOT-Mediated Increase in Stomatal Density Has No Impact on Photosynthetic Efficiency

SHORTROOT-Mediated Increase in Stomatal Density Has No Impact on Photosynthetic Efficiency

Arabidopsis BIRD Zinc Finger Proteins Jointly Stabilize Tissue Boundaries by Confining the Cell Fate Regulator SHORT-ROOT and Contributing to Fate Specification

SHORT-ROOT Regulates Primary, Lateral, and Adventitious Root Development in Arabidopsis

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