Physiologically active stomatal control originated at least as far back as the emergence of the Lycophytes

 

Land plants acquired active stomatal control early in their evolutionary history. 

by Ruszala E. M., Beerling D. J., Franks P. J., Chater C., Casson S. A., Gray J. E., Hetherington A. M. (2011)

Elizabeth M. Ruszala,

David J. Beerling,

Peter J. Franks,
Caspar Chater,
Stuart A. Casson,
Julie E. Gray,
Alistair M. Hetherington

===

in Curr Biol 2011,21:1030-1035 -DOI:

http://dx.doi.org/10.1016/j.cub.2011.04.044 –  

(PubMed Abstract | Publisher Full Text) – View ArticlePubMed

http://www.cell.com/current-biology/abstract/S0960-9822(11)00486-6?_returnURL=http%3A%2F%2Flinkinghub.elsevier.com%2Fretrieve%2Fpii%2FS0960982211004866%3Fshowall%3Dtrue 

https://www.sciencedirect.com/science/article/pii/S0960982211004866

Highlights

  • Active stomatal responses to CO2 and ABA are evolutionarily ancient
  • Active stomatal responses to CO2 and ABA are present in Selaginella
  • Stomata are a key evolutionary innovation vital to the success of the land plants

Summary

Stomata are pores that regulate plant gas exchange [ 1 ]. They evolved more than 400 million years ago [ 2, 3 ], but the origin of their active physiological responses to endogenous and environmental cues is unclear [ 2–6 ].

Recent research suggests that the stomata of lycophytes and ferns lack pore closure responses to abscisic acid (ABA) and CO2. This evidence led to the hypothesis that a fundamental transition from passive to active control of plant water balance occurred after the divergence of ferns 360 million years ago [ 7, 8 ].

Here we show that stomatal responses of the lycophyte Selaginella [ 9 ] to ABA and CO2 are directly comparable to those of the flowering plant Arabidopsis [ 10 ]. Furthermore, we show that the underlying intracellular signaling pathways responsible for stomatal aperture control are similar in both basal and modern vascular plant lineages.

Our evidence challenges the hypothesis that acquisition of active stomatal control of plant carbon and water balance represents a critical turning point in land plant evolution [ 7, 8 ].

Instead, we suggest that the critical evolutionary development is represented by the innovation of stomata themselves and that physiologically active stomatal control originated at least as far back as the emergence of the lycophytes (circa 420 million years ago) [ 11 ].

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Leaf Stomatal Traits of Trees in Relation to Gas Exchange

 

Variation in Leaf Stomatal Traits of 28 Tree Species in Relation to Gas Exchange along an Edaphic Gradient in a Bornean Rain Forest.

by Russo S.E., Cannon W. L., Elowsky C., Tan S., Davies, S. J. (2010)

  1. Sabrina E. Russo2,3,6,
  2. Whitney Logan Cannon2,
  3. Christian Elowsky4,
  4. Sylvester Tan3,5 and
  5. Stuart J. Davies3

Author Affiliations


  1. 2School of Biological Sciences, University of Nebraska, Lincoln, Nebraska 68588 USA

  2. 3Center for Tropical Forest Science–Arnold Arboretum Asia Program, Harvard University, Cambridge, Massachusetts 02138 USA

  3. 4Center of Biotechnology, University of Nebraska, Lincoln, Nebraska 68588 USA

  4. 5Forest Research Centre, Sarawak Forestry Corporation, Kuching, Sarawak, Malaysia

in American Journal of Botany, 97, 1109-1120. –

http://dx.doi.org/10.3732/ajb.0900344 – 

CrossRefPubMed – 

http://www.amjbot.org/content/97/7/1109

ABSTRACT

Premise of the study: Quantifying variation in functional traits associated with shifts in the species composition of plant communities along resource gradients helps identify environmental attributes important for community assembly. Stomates regulate the balance between carbon assimilation and water status in plants. If environmental attributes affecting photosynthetic water-use efficiency govern species distribution along an edaphic gradient, then adaptive variation in stomatal traits of plant species specializing on different soils should reflect belowground resource availability.

Methods: We tested this hypothesis by quantifying stomatal trait variation in understory saplings of 28 Bornean tree species in relation to gas exchange and water-use efficiency (WUE).

Key results: Comparisons between congeneric specialists of the more fertile, moister clay and the less fertile, well-drained sandy loam revealed little evidence of similar shifts in stomatal traits across genera, nor was stomatal pore index correlated with gmax, Amax, or WUE (Amax/gmax or Δ13C), suggesting that stomates may be overbuilt in these shaded juveniles. Amax was higher on sandy loam, likely due to higher understory irradiance there, but there were no other significant differences in gas exchange or WUE.

Conclusions: Despite substantial diversity in stomatal anatomy, there were few strong relationships between stomatal, photosynthetic, and WUE traits in relation to soil resources. Routine differences in water availability therefore may not exert a dominant control on the distributions of these Bornean tree species. Furthermore, the clades represented by these 12 genera may possess alternative functional designs enabling photosynthetic WUE that is sufficient to these humid, understory environments, due to whole plant-functional integration of stomatal traits with other, unmeasured traits influencing gas exchange.

 

All grass stomata with a four-cell configuration are more responsive to changing environmental conditions

170316151658_1_540x360
This image shows the four-celled stomata found in grasses, featuring two dumbbell-shaped guard cells surrounded by two subsidiary cells. Scientists attribute the tremendous success of grasses to this valve structure, which is capable of more-sensitive and precise responsiveness to the environment and likely enhances the plant’s performance, particularly in high temperatures or drought conditions. Credit: Dominique Bergmann and Michael Raissig – https://images.sciencedaily.com/2017/03/170316151658_1_540x360.jpg

 

How improved valves let grasses ‘breathe,’ cope with climate change

by Berry J. (2017)

Joseph Berry

Date:
March 16, 2017
Source:
Carnegie Institution for Science
Summary:
New work from a joint team of plant biologists and ecologists has uncovered the factor behind an important innovation that makes grasses — both the kind that make up native prairies and the kind we’ve domesticated for crops — among the most-common and widespread plants on the planet. Their findings may enable the production of plants that perform better in warmer and dryer climate conditions.

All land plants take in carbon dioxide (CO2) from the atmosphere and “exhale” oxygen and water vapor. This exchange is required for plant growth; the carbon dioxide is made into sugars by photosynthesis, the process by which plants turn the sun’s energy into food. But it also is a major driver of global climate cycles.

A plant needs to balance its ability to take in CO2 with the potential to lose water. To achieve this balance it uses tiny, cellular valve-like pores on the surfaces of its leaves called stomata (after the Greek word for mouths). In grasses, these valves are particularly well-tuned; they can open wide to maximize CO2 uptake and shut down quickly when the surrounding conditions would lead to increased water loss.

Because grass crops like corn, wheat, and rice are a major food source, the Carnegie-Stanford group wanted to know why the stomata in these particular plants work so much better than stomata in other plants. One obvious feature is that in most plants, stomata are made up of just two so-called “guard cells,” but grasses have an additional pair of cells on either side, which are called “subsidiary cells.” These subsidiary cells enable the guard cells to open and close especially quickly.

In addition, while the guard cells of many plants have a kidney shape, grass guard cells are an unusual “dumbbell” shape. The subsidiary cells alongside these dumbbell-resembling cells provide a mechanical boost to enable them to open wide.

In this study, led by Dominique Bergmann, an honorary adjunct staff member at Carnegie’s Department of Plant Biology and Professor at Stanford University’s Biology Department, the researchers used a relative of wheat called Brachypodium to demonstrate that all grass stomata with a four-cell configuration, including the two subsidiary cells, are indeed more responsive to changing environmental conditions, and have a wider range of apertures for pore opening and closing. This sensitivity likely enhances the plant’s performance, particularly in high temperatures or drought conditions.

Read the full article: Science Daily

RLK-mediated signaling in stomatal development

Photo credit: NCBI

Progression through the stomatal lineage and expression patterns of EPF, ERf and TMM genes

Depiction of the origin and progression of cells in the stomatal lineage of the leaf epidermis. Examples of divisions creating specific precursor cell types are shown in bulk on the growing leaf. Above each leaf stage are depicted two cells, one stomatal lineage and one not, and their development over time. The expression pattern of ligands (color coded shading as indicated in the key) follows their published transcriptional reporter expression. Receptors (depicted with the extracellular portion as a V-shape) are placed with their intracellular domains in the cell type corresponding to published transcriptional reporter expression. MMC, meristemoid mother cell; M, meristemoid, GC, guard cell.

Complex signals for simple cells: the expanding ranks of signals and receptors guiding stomatal development.

by Rowe M. H., Bergmann D. C. (2010)

 

Department of Biology, Stanford University, Stanford, CA 94305-5020, USA.

in Curr. Opin. Plant Biol. 2010 Oct;13(5):548-55.- doi: 10.1016/j.pbi.2010.06.002. Epub 2010 Jul 16. –

PMID: 20638894 – 

https://www.ncbi.nlm.nih.gov/pubmed?Db=pubmed&Cmd=ShowDetailView&TermToSearch=20638894

Abstract

In development, pattern formation requires that cell proliferation and differentiation be precisely coordinated. Stomatal development has served as a useful model system for understanding how this is accomplished in plants. Although it has been known for some time that stomatal development is regulated by a family of receptor-like kinases (RLKs) and an accompanying receptor-like protein (RLP), only recently have putative ligands been identified.

Despite the structural homology demonstrated by the genes that encode these small, secreted peptides, they convey different information, vary with one another in their relationship to common signaling components, control distinct aspects of stomatal development, and do so antagonistically.

Their discovery has revealed the intricate network of interactions required upstream of RLK signal transduction for the patterning of complex tissues. However, at issue still is whether specific ligand-receptor combinations are responsible for the activation of discrete signaling pathways or spatiotemporal modulation of a common pathway.

This review integrates the latest findings regarding RLK-mediated signaling in stomatal development with emerging paradigms in the field.

Grass stomata and climate change

 

Photo credit: Manila Bulletin

Wheat and other edible grasses have developed pores that make them more drought tolerant. Stanford scientists have studied these pores with an eye toward future climate change. (Image credit: magdasmith / Getty Images) | credit Stanford University | Manila Bulletin

Grass stomata seen as possible lead to crops better surviving climate change

By Philippine News Agency

The increased efficiency of grass stomata, as confirmed in a new study, may lead to crops that can better survive climate change.

Wheat and other edible grasses have developed pores that make them more drought tolerant. Stanford scientists have studied these pores with an eye toward future climate change. (Image credit: magdasmith / Getty Images) | credit Stanford University | Manila Bulletin

Stomata, the holes in the leaves of land-based plants through which they take in carbon dioxide (CO2) and let out oxygen and water vapor, have remained largely unchanged in the 400 million years since plants colonized the land, according to a resarch paper published in the March 17 issue of the journal Science.

One major exception is grasses, which are better able to withstand drought or high temperatures in large part due to changes in their stomata.

Stomata usually have two so-called “guard cells” with a hole in the middle that opens and closes depending on how a plant needs to balance its gas exchange. If a plant needs more CO2 or wants to cool by releasing water vapor, the stomata open. If it needs to conserve water, they stay closed.

Grasses, which include wheat, corn and rice and make up about 60 percent of the calories people consume worldwide, improved on the original structure by recruiting two extra cells on either side of the guard cells, allowing for a little extra give when the stoma opens. They also respond more rapidly and sensitively to changes in light, temperature or humidity that happen during the day.

The different stomata may have helped grasses spread during a prehistoric period of increased global dryness.

Scientists have assumed grasses’ unusual stomata make these plants more efficient “breathers.” But, spurred by curiosity and a passion for developmental biology, researchers at Stanford University decided to test that theory.

The researchers of the study said they found a mutant of the wheat relative Brachypodium distachyon that had two-celled stomata, compared the stomata from the mutant to the normal four-celled stomata, and confirmed that the four-celled version opens wider and faster.

In addition, they identified which gene creates the four-celled stomata.

Read the full story: Manila Bulletin

Subsidiary cells to build physiologically improved grass stomata

 

Mobile MUTE specifies subsidiary cells to build physiologically improved grass stomata

Raissig M. T., Matos J. L., Anleu Gil M. X., Kornfeld A., Bettadapur A., Abrash E., Allison H. R., Badgley G., Vogel J. P., Berry J. A., Bergmann D. C. (2017)

  1. Michael T. Raissig1,*,
  2. Juliana L. Matos1,
  3. M. Ximena Anleu Gil2,
  4. Ari Kornfeld3,
  5. Akhila Bettadapur2,
  6. Emily Abrash1,
  7. Hannah R. Allison1,
  8. Grayson Badgley3,
  9. John P. Vogel4,
  10. Joseph A. Berry3,
  11. Dominique C. Bergmann1,2,*

  1. 1Department of Biology, Stanford University, 371 Serra Mall, Stanford, CA 94305, USA.

  2. 2Howard Hughes Medical Institute (HHMI), Stanford University, 371 Serra Mall, Stanford, CA 94305, USA.

  3. 3Department of Global Ecology, Carnegie Institution for Science, 260 Panama Street, Stanford, CA 94305, USA.

  4. 4U.S. Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598, USA.

in Science  17 Mar 2017: Vol. 355, Issue 6330, pp. 1215-1218 – DOI: 10.1126/science.aal3254

http://science.sciencemag.org/content/355/6330/1215?rss=1

Making more of your stomata

Stomata on grasses are made up of two guard cells and two subsidiary cells, and they perform better than stomata on broad-leaved plants, which are made up only of two guard cells. Raissig et al. found that the MUTE transcription factor in the wheat-like grass Brachypodium is a little bigger than the equivalent protein in the model broad-leaved plant Arabidopsis. The extension in the grass protein promotes its movement into adjacent cells, prompting them to become subsidiary cells. Mutant Brachypodium whose MUTE protein could not move between cells lacked stomatal subsidiary cells and grew poorly.

Abstract

Plants optimize carbon assimilation while limiting water loss by adjusting stomatal aperture. In grasses, a developmental innovation—the addition of subsidiary cells (SCs) flanking two dumbbell-shaped guard cells (GCs)—is linked to improved stomatal physiology.

Here, we identify a transcription factor necessary and sufficient for SC formation in the wheat relative Brachypodium distachyon. Unexpectedly, the transcription factor is an ortholog of the stomatal regulator AtMUTE, which defines GC precursor fate in Arabidopsis.

The novel role of BdMUTE in specifying lateral SCs appears linked to its acquisition of cell-to-cell mobility in Brachypodium. Physiological analyses on SC-less plants experimentally support classic hypotheses that SCs permit greater stomatal responsiveness and larger range of pore apertures.

Manipulation of SC formation and function in crops, therefore, may be an effective approach to enhance plant performance.

Science, this issue p. 1215

Stomatal spacing and dynamic two-way interactions between stem cells and their neighborhood

nihms386856f2
Patterns observed among lineages involving more than two rounds of division (47 lineages analyzed). Interpretive diagrams (A,C,E) are shown above time-lapse confocal images (B,D,F). (A) P cell undergoes 2–3 divisions in alternating orientations, followed by a division across adjacent walls (21 lineages). The result is a spiral arrangement. (C) As A except that two successive divisions span adjacent walls (10 lineages). (E) Two parallel divisions prior to an alternating division and then a final division that joins adjacent walls (3 lineages). The remaining 13 lineages corresponded to truncated versions of the above three patterns. Red = P cells, yellow = N cells, Scale bars (white lines) are 10μm. – https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3383840/bin/nihms386856f2.jpg

Generation of spatial patterns through cell polarity switching

by Robinson S. J., Barbier de Reuille P., Bergmann D. C., Prusinkiewicz P., Coen E. (2011)

John Innes Centre, Norwich Research Park, Colney, Norwich NR4 7UH, UK.

in Science 333(6048):1436-40 – doi: 10.1126/science.1202185. –

PMID: 21903812 – 

https://www.ncbi.nlm.nih.gov/pubmed/21903812

Abstract

The mechanisms that generate dynamic spatial patterns within proliferating tissues are poorly understood, largely because of difficulties in unravelling interactions between cell specification, polarity, asymmetric division, rearrangements, and growth.

We address this problem for stomatal spacing in plants, which offer the simplifying advantage that cells do not rearrange. By tracking lineages and gene activities over extended periods, we show that limited stem cell behavior of stomatal precursors depends on maintenance of the SPEECHLESS (SPCH) transcription factor in single daughter cells.

Modeling shows how this property can lead to observed stereotypical stomata lineages through a postmitotic polarity-switching mechanism. The model predicts the location of a polarity determinant BASL over multiple divisions, which we validate experimentally.

Our results highlight the dynamic two-way interactions between stem cells and their neighborhood during developmental patterning.