Short-Root1 Plays a Role in the Development of Vascular Tissue and Kranz Anatomy in Maize Leaves

Slewinski, Thomas L.; Anderson, Alyssa A.; Price, Simara; Withee, Jacob R.; Gallagher, Kimberly L.; Turgeon, Robert

doi:10.1093/mp/ssu036

Cited by 58 publications

(54 citation statements)

References 14 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%

“…5B) lines, suggesting that neither ectopic ZmSHR1 activity nor the presence of supernumerary stomatal files caused any gross alterations in shoot anatomy. To confirm this observation, particularly given that loss-of-function mutations in shr1 in maize are reported to perturb vein spacing and the specification of bundle sheath cells (Slewinski et al, 2014), a range of leaf anatomy traits also were quantified. Table I shows measurements of leaf width, leaf length, total number of longitudinal veins, bundle sheath cell size, cell number, and distance between veins for four individuals of each T2 line and the wild type.…”

Section: The Development Of Supernumerary Stomata Has No Significant mentioning

confidence: 99%

“…In maize, ZmSHR2 and its homeolog ZmSHR2h have both been retained in the genome, whereas only one copy of ZmSHR1 is present. The published nomenclature for these genes is somewhat confusing, because the ZmSHR1 sequence (GRMZM2G132794; Slewinski et al, 2014) is orthologous to OsSHR2 (Os03g31880), and the homeologs ZmSHR2 (GRMZM2G172657) and ZmSHR2h (GRMZM2G019060) Figure 1. Phylogenetic tree of SHR-like proteins.…”

Section: Duplicate Shr Genes In Grassesmentioning

confidence: 99%

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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%

Section: The Development Of Supernumerary Stomata Has No Significant mentioning

confidence: 99%

Section: Duplicate Shr Genes In Grassesmentioning

confidence: 99%

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

et al. 2017

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“…The evolution of this modified photosynthetic pathway represents a wonderful example of convergent evolution. While the changes necessary for the transition from C 3 to C 4 photosynthesis are numerous, the trait has a wide phylogenetic distribution across angiosperms, with 19 families across the globe known to contain one or multiple members capable of C 4 photosynthesis [2]. Much research on eudicot C 4 has focused on Flaveria species (Asteraceae), which contains not only C 4 species but also a number of C 3 /C 4 intermediates [3].…”

Section: Introductionmentioning

confidence: 99%

Gene and genome duplications and the origin of C4 photosynthesis: Birth of a trait in the Cleomaceae

Bergh

Külahoglu

Bräutigam

et al. 2014

Current Plant Biology

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a b s t r a c t C 4 photosynthesis is a trait that has evolved in 66 independent plant lineages and increases the efficiency of carbon fixation. The shift from C 3 to C 4 photosynthesis requires substantial changes to genes and gene functions effecting phenotypic, physiological and enzymatic changes. We investigate the role of ancient whole genome duplications (WGD) as a source of new genes in the development of this trait and compare expression between paralog copies. We compare Gynandropsis gynandra, the closest relative of Arabidopsis that uses C 4 photosynthesis, with its C 3 relative Tarenaya hassleriana that underwent a WGD named Th-␣. We establish through comparison of paralog synonymous substitution rate that both species share this paleohexaploidy. Homologous clusters of photosynthetic gene families show that gene copy numbers are similar to what would be expected given their duplication history and that no significant difference between the C 3 and C 4 species exists in terms of gene copy number. This is further confirmed by syntenic analysis of T. hassleriana, Arabidopsis thaliana and Aethionema arabicum, where syntenic region copy number ratios lie close to what could be theoretically expected. Expression levels of C 4 photosynthesis orthologs show that regulation of transcript abundance in T. hassleriana is much less strictly controlled than in G. gynandra, where orthologs have extremely similar expression patterns in different organs, seedlings and seeds. We conclude that the Th-␣ and older paleopolyploidy events have had a significant influence on the specific genetic makeup of Cleomaceae versus Brassicaceae. Because the copy number of various essential genes involved in C 4 photosynthesis is not significantly influenced by polyploidy combined with the fact that transcript abundance in G. gynandra is more strictly controlled, we also conclude that recruitment of existing genes through regulatory changes is more likely to have played a role in the shift to C 4 than the neofunctionalization of duplicated genes. DATA: The data deposited at NCBI represents raw RNA reads for each data series mentioned: 5 leaf stages, root, stem, stamen, petal, carpel, sepal, 3 seedling stages and 3 seed stages of Tarenaya hassleriana and Gynandropsis gynandra. The assembled reads were used for all analyses of this paper where RNA was used. http://www.ncbi.nlm.nih.gov/Traces/sra/?study=SRP036637, http://www.ncbi.nlm.nih.gov/ Traces/sra/?study=SRP036837 den Bergh), canan.kuelahoglu@uni-duesseldorf.de (C. Külahoglu), andrea.braeutigam@uni-duesseldorf.de (A. Bräutigam), jmh65@cam.ac.uk (J.M. Hibberd), andreas.weber@uni-duesseldorf.de (A.P.M. Weber), zhuxinguang@picb.ac.cn (X.-G. Zhu), eric.schranz@wur.nl (M. Eric Schranz).

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“…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).…”

Section: Introductionmentioning

confidence: 98%

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

Bergh

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Erik van den Bergh4. Fabricated 'truths' in spite of scientific observations and conclusions show a lack of understanding, not a lack of goodwill.5. What brings people together is not a good speech, but a good listen.6. Parenthood is about guiding the next generation and forgiving the last.Propositions belonging to the thesis entitled: "Comparative genomics and trait evolution in Cleomaceae, a model family for ancient

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Short-Root1 Plays a Role in the Development of Vascular Tissue and Kranz Anatomy in Maize Leaves

Cited by 58 publications

References 14 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

Gene and genome duplications and the origin of C4 photosynthesis: Birth of a trait in the Cleomaceae

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

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