Stomatal development in the grasses

Stomatal development: focusing on the grasses

by Hepworth C., Caine R. S., Harrison E. L., Sloan J., Gray J. E. (2018)

Christopher Hepworth1, Robert S. Caine2, Emily L. Harrison2, Jennifer Sloan, Julie E. Gray2

1 Department of Animal and Plant Sciences, University of Sheffield, S10 2TN, UK

2 Department of Molecular Biology and Biotechnology, University of Sheffield, S10 2TN, UK

===

In Current Opinion Plant Biology 41: 1-7 – https://doi.org/10.1016/j.pbi.2017.07.009

https://www.sciencedirect.com/science/article/pii/S1369526617300997

Highlights

• Grass stomatal complexes differ from those of dicots.

Grasses form rows of dumbbell-shaped guard cell pairs flanked by subsidiary cells.

• Grasses and dicots share differently regulated orthologous transcription factors.

• Both grasses and dicots use epidermal patterning factor family signaling peptides.

• Manipulation of epidermal patterning factors enhances cereal water use efficiency.

Abstract

The development and patterning of stomata in the plant epidermis has emerged as an ideal system for studying fundamental plant developmental processes.

Over the past twenty years most studies of stomata have used the model dicotyledonous plant Arabidopsis thaliana. However, cultivated monocotyledonous grass (or Gramineae) varieties provide the majority of human nutrition, and future research into grass stomata could be of critical importance for improving food security.

Recent studies using Brachypodium distachyonHordeum vulgare (barley) and Oryza sativa (rice) have led to the identification of the core transcriptional regulators essential for stomatal initiation and progression in grasses, and begun to unravel the role of secretory signaling peptides in controlling stomatal developmental.

This review revisits how stomatal developmental unfolds in grasses, and identifies key ontogenetic steps for which knowledge of the underpinning molecular mechanisms remains outstanding.

Bacterial infection systemically suppresses stomatal density

Bacterial infection systemically suppresses stomatal density

by Dutton C., Hörak H., Hepworth C., Mitchell A., Ton J., Hunt L., Gray J. E. (2019)

Christian Dutton, Hanna Hõrak, Christopher Hepworth,Alice Mitchell, Jurriaan Ton, Lee Hunt, Julie E. Gray,

Department of Molecular Biology and Biotechnology, University of Sheffield, UK

===

In Plant, Cell & Environment https://doi.org/10.1111/pce.13570 –

https://onlinelibrary.wiley.com/doi/abs/10.1111/pce.13570?af=R

Abstract

Many plant pathogens gain entry to their host via stomata. On sensing attack, plants close these pores to restrict pathogen entry.

Here, we show that plants exhibit a second longer‐term stomatal response to pathogens. Following infection, the subsequent development of leaves is altered via a systemic signal. This reduces the density of stomata formed, thus providing fewer entry points for pathogens on new leaves. Arabidopsis thaliana leaves produced after infection by a bacterial pathogen that infects through the stomata (Pseudomonas syringae) developed larger epidermal pavement cells and stomata, and consequently had up to 20% reductions in stomatal density.

The bacterial peptide flg22 or the phytohormone salicylic acid induced similar systemic reductions in stomatal density suggesting that they might mediate this effect. In addition, flagellin receptors, salicylic acid accumulation, and the lipid transfer protein AZI1 were all required for this developmental response.

Furthermore, manipulation of stomatal density affected the level of bacterial colonisation, and plants with reduced stomatal density showed slower disease progression.

We propose that following infection, development of new leaves is altered by a signalling pathway with some commonalities to systemic acquired resistance. This acts to reduce the potential for future infection by providing fewer stomatal openings.

Stomatal development: key ontogenetic steps for which knowledge of the underpinning molecular mechanisms remains outstanding

Stomatal development: focusing on the grasses

by Hepworth C., Caine R. S., Harrison E. L., Sloan J., Gray J. E. (2018)

Christopher Hepworth, 1,

Robert S. Caine, 2,

Emily L. Harrison, 2,

Jennifer Sloan, 12,

Julie E. Gray, 2

Department of Animal and Plant Sciences, University of Sheffield, S10 2 TN, UK

2Department of Molecular Biology and Biotechnology, University of Sheffield, S10 2TN, UK

===

In Current Opinion in Plant Biology 41: 1-7 – https://doi.org/10.1016/j.pbi.2017.07.009 – 

https://www.sciencedirect.com/scie nce/article/pii/S1369526617300997

Abstract

Highlights

  • Grass stomatal complexes differ from those of dicots.•
  • Grasses form rows of dumbbell-shaped guard cell pairs flanked by subsidiary cells.
  • Grasses and dicots share differently regulated orthologous transcription factors.

The development and patterning of stomata in the plant epidermis has emerged as an ideal system for studying fundamental plant developmental processes. Over the past twenty years most studies of stomata have used the model dicotyledonous plant Arabidopsis thaliana.

However, cultivated monocotyledonous grass (or Gramineae) varieties provide the majority of human nutrition, and future research into grass stomata could be of critical importance for improving food security.

Recent studies using Brachypodium distachyonHordeum vulgare (barley) and Oryza sativa (rice) have led to the identification of the core transcriptional regulators essential for stomatal initiation and progression in grasses, and begun to unravel the role of secretory signaling peptides in controlling stomatal developmental.

This review revisits how stomatal developmental unfolds in grasses, and identifies key ontogenetic steps for which knowledge of the underpinning molecular mechanisms remains outstanding.

Manipulating stomatal density enhances drought tolerance

Manipulating stomatal density enhances drought tolerance without deleterious effect on nutrient uptake

by Hepworth C., Adams T. D., Hunt L., Cameron D. D., Gray J. E. (2015)

===

in New Phytologist 2: 336-341 – doi: 10.1111/nph.13598 –

Summary

  • Manipulation of stomatal density was investigated as a potential tool for enhancing drought tolerance or nutrient uptake.
  • Drought tolerance and soil water retention were assessed using Arabidopsis epidermal patterning factor mutants manipulated to have increased or decreased stomatal density. Root nutrient uptake via mass flow was monitored under differing plant watering regimes using nitrogen‐15 (15N) isotope and mass spectrometry.
  • Plants with less than half of their normal complement of stomata, and correspondingly reduced levels of transpiration, conserve soil moisture and are highly drought tolerant but show little or no reduction in shoot nitrogen concentrations especially when water availability is restricted. By contrast, plants with over twice the normal density of stomata have a greater capacity for nitrogen uptake, except when water availability is restricted.
  • We demonstrate the possibility of producing plants with reduced transpiration which have increased drought tolerance, with little or no loss of nutrient uptake. We demonstrate that increasing transpiration can enhance nutrient uptake when water is plentiful.

Plants can balance water uptake and loss through coordinated regulation of both stomatal and root development

Screen Shot 2018-03-31 at 17.24.12
Fig 2. Stomatal density correlates with root area. (A) Histochemical staining of seedlings expressing pEPF1::GUS (top) indicates EPF1 expression in guards cells but not in roots, and pEPF2::GUS (bottom) indicates EPF2 expression in early stomatal lineage cells and not in roots. (B) Representative scans to illustrate root size of plants grown in rhizotrons. (C) Linear regression showing a significant relationship between stomatal density and the rooting area of plants grown in rhizotrons (P = 0.0083). (D) Increased root hair length in plants with increased stomatal density. (E) Increased root hair density in plants with increased stomatal density. (F) Representative micrographs of plants grown in agar to assess root hair length and density. Bars with no letters in common are significantly different, P<0.05, (Tukeys test after one-way ANOVA). Error bars represent SE.

 

Balancing water uptake and loss through the coordinated regulation of stomatal and root development

by Hepworth C., Turner C., Landim M. G.,  Cameron D.D., Gray J. E. (2015)

===

in PloS one 11 (6), e0156930 – https://doi.org/10.1371/journal.pone.0156930 –

http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0156930

Abstract

Root development is influenced by nutrient and water availabilities. Plants are able to adjust many attributes of their root in response to environmental signals including the size and shape of the primary root, lateral roots and root hairs.

Here we investigated the response of roots to changes in the levels of leaf transpiration associated with altered stomatal frequency.

We found that plants with high stomatal density and conductance produce a larger rooting area and as a result have enhanced phosphate uptake capacity whereas plants with low stomatal conductance produce a smaller root.

Manipulating the growth environment of plants indicated that enhanced root growth is most likely a result of an increased demand for water rather than phosphate. Plants manipulated to have an increase or reduction in root hair growth show a reduction or increase respectively, in stomatal conductance and density.

Our results demonstrate that plants can balance their water uptake and loss through coordinated regulation of both stomatal and root development.

Insights into how grasses regulate the production of stomata

1-s2.0-S1369526617300997-fx1_lrg

 

Stomatal development: focusing on the grasses

by Hepworth C., Caine R. S., Harrison E. L., Sloan J., Gray J. E. (2016)

Christopher Hepworth, 1  Robert S. Caine, 2  Emily L. Harrison, 2  Jennifer Sloan, 12   Julie E. Gray, 2

1
Department of Animal and Plant Sciences, University of Sheffield, S10 2TN, UK
2
Department of Molecular Biology and Biotechnology, University of Sheffield, S10 2TN, UK

==================================

in Current Opinion in Plant Biology 41: 1-7 – https://doi.org/10.1016/j.pbi.2017.07.009 – 

https://www.sciencedirect.com/science/article/pii/S1369526617300997

Highlights

Grass stomatal complexes differ from those of dicots.

Grasses form rows of dumbbell-shaped guard cell pairs flanked by subsidiary cells.

Grasses and dicots share differently regulated orthologous transcription factors.

Both grasses and dicots use epidermal patterning factor family signaling peptides.

Manipulation of epidermal patterning factors enhances cereal water use efficiency.

The development and patterning of stomata in the plant epidermis has emerged as an ideal system for studying fundamental plant developmental processes. Over the past twenty years most studies of stomata have used the model dicotyledonous plant Arabidopsis thaliana.

However, cultivated monocotyledonous grass (or Gramineae) varieties provide the majority of human nutrition, and future research into grass stomata could be of critical importance for improving food security.

Recent studies using Brachypodium distachyonHordeum vulgare (barley) and Oryza sativa (rice) have led to the identification of the core transcriptional regulators essential for stomatal initiation and progression in grasses, and begun to unravel the role of secretory signaling peptides in controlling stomatal developmental.

This review revisits how stomatal developmental unfolds in grasses, and identifies key ontogenetic steps for which knowledge of the underpinning molecular mechanisms remains outstanding.

The potential of manipulating stomatal frequency

 

 

Reducing stomatal density in barley improves drought tolerance without impacting on yield.

by Hughes J., Hepworth C., Dutton C., Dunn J. A., Hunt L., Stephens J., Waugh R., Cameron D. D., Gray J. E. (2017)

Jonathan HughesChristopher HepworthChristian DuttonJessica A. DunnLee HuntJennifer StephensDuncan CameronRobbie WaughJulie E Gray,

in Plant Physiol. 174: 776–787 – DOI: https://doi.org/10.1104/pp.16.01844

http://www.plantphysiol.org/content/early/2017/05/01/pp.16.01844

Abstract

The epidermal patterning factor (EPF) family of secreted signalling peptides regulate the frequency of stomatal development in model dicot and basal land plant species.

Here we identify and manipulate the expression of a barley ortholog and demonstrate that when overexpressed HvEPF1 limits entry to, and progression through, the stomatal development pathway.

Despite substantial reductions in leaf gas exchange, barley plants with approximately half of the normal number of stomata show no reductions in grain yield. In addition, HvEPF1OE barley lines exhibit significantly enhanced water use efficiency, drought tolerance and soil water conservation properties.

Our results demonstrate the potential of manipulating stomatal frequency for the protection and optimisation of cereal crop yields under future drier environments.