Candidate regulators of Early Leaf Development in Maize Perturb Hormone Signalling and Secondary Cell Wall Formation When Constitutively Expressed in Rice

Wang, Peng; Karki, Shanta; Biswal, Akshaya Kumar; Lin, Hsiang-Chun; Jacqueline, Dionora, Mary; Rizal, Govinda; Yin, Xiaojia; Schuler, Mara; Hughes, Thomas E; Fouracre, Jim P.; Jamous, Basel Abu; Sedelnikova, Olga V.; Lo, Shuen‐Fang; Bandyopadhyay, Anindya; Yu, Su‐May; Kelly, Steven L.; Quick, W. Paul; Langdale, Jane A.

doi:10.1038/s41598-017-04361-w

Cited by 19 publications

(16 citation statements)

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“…The distinct expression pattern of OsSCR during guard cell and subsidiary cell formation in the rice epidermis predicts a further role for SCR in stomatal formation (Kamiya et al, 2003). However, ectopic expression of ZmSCR1 in rice does not perturb stomatal density or patterning, at least when expressed constitutively and at high levels (Wang et al, 2017). Therefore, stomatal specification must be mediated by interactions with alternative downstream targets, the most likely candidates being homologs of BdSPCH and BdICE, which have been shown to act in the earliest stages of specification in B. distachyon (Raissig et al, 2016).…”

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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“…Establishment of a C 4 vascular system is likely to be under complex genetic control. Sixty known developmental regulators from maize (C 4 ) were constitutively expressed individually in rice (C 3 ), but no single gene conferred increased vein density (Wang et al ., ), indicating that multiple mutations might be needed. Decades earlier, putative mutants with disrupted venation were induced in the C 4 species Panicum maximum (also known as Megathyrsus maximus ) (Fladung, ).…”

Section: Molecular and Genetic Mechanisms Of C4 Leaf Venationmentioning

confidence: 99%

“…Transcriptomic data are consistent with this presumed function. However, constitutive expression of SCR1 in rice had no effect (Wang et al ., ), indicating that SCR1 by itself is insufficient for alterations in vein development.…”

Section: Molecular and Genetic Mechanisms Of C4 Leaf Venationmentioning

confidence: 99%

Getting closer: vein density in C₄ leaves

Kumar

Kellogg

2018

New Phytologist

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Contents Summary1260I.Introduction1260II.Molecular and genetic mechanisms of C4 leaf venation1262III.Conclusions and future perspectives1266Acknowledgements1266References1266 Summary C4 grasses are major contributors to the world's food supply. Their highly efficient method of carbon fixation is a unique adaptation that combines close vein spacing and distinct photosynthetic cell types. Despite its importance, the molecular genetic basis of C4 leaf development is still poorly understood. Here we summarize current knowledge of leaf venation and review recent progress in understanding molecular and genetic regulation of vascular patterning events in C4 plants. Evidence points to the interplay of auxin, brassinosteroids, SHORTROOT/SCARECROW and INDETERMINATE DOMAIN transcription factors. Identification and functional characterization of candidate regulators acting early in vascular development will be essential for further progress in understanding the precise regulation of these processes.

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“…It could be shown that SCARECROW and SHORT-ROOT mutants of maize as well as Arabidopsis thaliana exhibit distorted bundle sheath development (Slewinski et al, 2012, 2014; Cui et al, 2014). The overexpression of the maize SCARECROW gene ( ZmSCR1 ) in Kitaake rice, on the other hand, did not lead to remarkable changes in leaf anatomy (Wang et al, 2017a).…”

Section: Introductionmentioning

confidence: 99%

Transcriptome dynamics in developing leaves from C₃and C₄Flaveriaspecies reveal determinants of Kranz anatomy

Billakurthi

Wrobel

Bräutigam

et al. 2018

Preprint

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C4 species have evolved more than 60 times independently from C3 ancestors. This multiple and parallel evolution of the complex C4 trait indicates common underlying evolutionary mechanisms that might be identified by comparative analysis of closely related C3 and C4 species. Efficient C4 function depends on a distinctive leaf anatomy that is characterized by enlarged, chloroplast rich bundle sheath cells and a narrow vein spacing. To elucidate molecular mechanisms generating this so called Kranz anatomy, we analyzed a developmental series of leaves from the C4 plant Flaveria bidentis and the closely related C3 species Flaveria robusta using leaf clearing and whole transcriptome sequencing. Applying non-negative matrix factorization on the data identified four different zones with distinct transcriptome patterns in growing leaves of both species. Comparing these transcriptome patterns revealed an important role of auxin metabolism and especially auxin homeostasis for establishing the high vein density typical for C4 leaves.2012). Under current ambient CO2 concentrations (405 ppm) at 25°C, photorespiration is estimated to decrease the yield of soybean or wheat in the US by 36% and 20%, respectively (Walker et al., 2016). Environmental constrains such as high temperatures and drought further increases Rubisco oxygenase activity (Laing et al., 1974; Jordan and Ogren, 1984; Brooks and Farquhar, 1985; Parry et al., 2007).In most C4 plants CO2 fixation is compartmentalized between two cell types, the bundle sheath (BS) and the mesophyll (M) cells. In the mesophyll phosphoenolpyruvate (PEP) is carboxylated by phosphoenolpyruvate carboxylase (PEPC), resulting in the 4-carbon compound oxaloacetate (OAA). OAA is converted to malate and/or aspartate, which is then transferred to the bundle sheath. Here the 4-carbon compounds are decarboxylated and the released CO2 is assimilated in the Calvin-Benson-Bassham cycle (CBB). The resulting pyruvate is transferred back to the mesophyll where the primary CO2 acceptor PEP is regenerated by pyruvate orthophosphate dikinase (PPDK) (Hatch, 1987).C4 photosynthesis requires a particular leaf anatomy. As BS and M cells operate as a photosynthetic unit, direct contact of both cell types is necessary to ensure efficient photosynthesis.The BS is composed of the cells directly adjacent to the vasculature. Therefore, leaves of most C4 species exhibit high vein densities with a characteristic pattern in which two veins, each surrounded by BS cells, are separated by only two layers of M cells in a vein-bundle sheathmesophyll-mesophyll-bundle sheath-vein layout. Bundle sheath cells of C4 plants often appear larger in cross-section compared to C3 species and contain more chloroplasts. This character-

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Candidate regulators of Early Leaf Development in Maize Perturb Hormone Signalling and Secondary Cell Wall Formation When Constitutively Expressed in Rice

Cited by 19 publications

References 57 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

Getting closer: vein density in C₄ leaves

Transcriptome dynamics in developing leaves from C₃and C₄Flaveriaspecies reveal determinants of Kranz anatomy

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Candidate regulators of Early Leaf Development in Maize Perturb Hormone Signalling and Secondary Cell Wall Formation When Constitutively Expressed in Rice

Cited by 19 publications

References 57 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

Getting closer: vein density in C4 leaves

Transcriptome dynamics in developing leaves from C3and C4Flaveriaspecies reveal determinants of Kranz anatomy

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Getting closer: vein density in C₄ leaves

Transcriptome dynamics in developing leaves from C₃and C₄Flaveriaspecies reveal determinants of Kranz anatomy