Blatt, Michael R.

Cai, Shengguan

Chen, Zhong-Hua

Papanatsiou, Maria

English

Shengguan Cai

Maria Papanatsiou

Michael R. Blatt

Zhong-Hua Chen

Crossref

Molecular Plant

Speedy Grass Stomata: Emerging Molecular and Evolutionary Features

Enlighten: Publications

Molecular Plant
SpotlightSpeedy Grass Stomata: Emerging Molecular and
Evolutionary FeaturesPublished by the Molecular Plant Shanghai Editorial Office in association with
Cell Press, an imprint of Elsevier Inc., on behalf of CSPB and IPPE, SIBS, CAS.Stomata in most land plants are formed by a pair of guard cells,
controlling the water loss and the carbon dioxide uptake. The
development, patterning, and density of stomata are funda-
mental traits for stomatal function, contributing to plant growth
and productivity (Pillitteri and Torii, 2012). The stomata of most
plant species consist of two kidney-shaped guard cells, while
stomata of grass species are formed by two dumbbell-shaped
guard cells flanked by two subsidiary cells (Figure 1A). The
four-celled stomatal complex in grasses may facilitate a fast
response to environmental cues for efficient photosynthesis
and water use, possibly through the rapid transport of ions and
osmolytes between guard cells and subsidiary cells (see Jezek
and Blatt, 2017; Chen et al., 2017 and references therein).
Given that many grasses are agronomically important species
as staple food, feed, and biofuel sources, it is vital to
understand the molecular mechanisms of grass stomata
development and patterning, and of membrane transport in
guard cells and subsidiary cells, which govern the opening and
closure of stomatal pores.
Our understanding of the genetic control of stomata develop-
ment in the model grass species Brachypodium distachyon
has been advanced by two recent groundbreaking studies by
Raissig et al. (2016, 2017). The authors investigated the roles
and functions of inducer of CBF expression (ICE)/SCREAM
(SCRM) basic helix-loop-helix (bHLH) and SPEECHLESS
(SPCH), MUTE, and FAMA-like bHLHs in the model grass
B. distachyon by using mutagenesis, genome editing, and other
emerging technologies. Their most exciting discovery is that
BdMUTE acts as one of the key regulators for subsidiary cell
formation and proper guard mother cell division. A 5-bp deletion
in BdMUTE led to a failure in recruitment of subsidiary cells, and
rendered stomata with only two guard cells in the subsidiary cell
identity defective (sid) mutant, which could be complemented
by BdMUTEp:BdMUTE. BdMUTE protein was detected in
both guard cells and subsidiary cells, but intriguingly BdMUTE
gene is expressed in guard mother cells, suggesting that
BdMUTE protein moves from guard mother cells into subsidiary
mother cells, probably via plasmodesmata. The loss of subsid-
iary cells in sid could not be rescued by the introduction of
BdMUTEp:AtMUTE, suggesting that mobility is an intrinsic
feature of BdMUTE protein and is essential for subsidiary cell
patterning in grasses. In the model eudicot Arabidopsis, the
development of Arabidopsis stomata depends on group Ia
bHLH transcription factors—AtSPCH, AtMUTE, and AtFAMA—
in heterodimeric association with bHLH group IIIb partners,
AtICE1 and AtSCRM2 (Pillitteri and Torii, 2012; Chater
et al., 2017). Although many key genes regulating stomatal
development and patterning have been identified and
extensively studied in Arabidopsis (Pillitteri and Torii, 2012;
Chater et al., 2017), the discovery of grass-specific function of
their homologous genes has major implications for plant and
agricultural science and evolutionary biology.912 Molecular Plant 10, 912–914, July 2017 ª The Author 2017.
This is an open access article under the CC BY license (http://creGrass stomata are unique in nearly all aspects of their physiology
and development compared with non-monocot plant stomata:
they show faster stomatal responses, distinct morphological
and structural features, and unique membrane transport and
signaling systems. We hypothesized that the success of grass
is likely attributed to the evolution of highly responsive stomata
capable of maximizing productivity in rapidly changing environ-
ments; grass stomata harness the active turgor control mecha-
nisms present in stomata of more ancient plant lineages,
maximizing several morphological and developmental features
to ensure rapid responses to environmental inputs (Chen et al.,
2017 and references therein). This hypothesis is supported
by the work on subsidiary cell-less sid mutant in Raissig
et al. (2017). These authors found that the maximum pore
area of stomata in sid mutant was only half of that in the wild-
type, even when forced open by the toxin fusicoccin. The sid
mutant showed slower stomatal responses to changing light
intensities, and its stomata exhibited a reduced dynamic range
of apertures compared with the wild-type. Most importantly,
the sid mutant produced less biomass than the wild-type,
linking BdMUTE-regulated subsidiary cell formation with impact
on photosynthesis and biomass production in a grass species.
The findings also suggest that engineering the properties of the
subsidiary cell may allow for fine-tuning stomatal responses,
which affect photosynthesis, water use efficiency, and crop
yield.
The early acquisition of stomata is fundamentally important for
the evolution of land plants, and many key genes encoding sto-
matal functions have been conserved since the first stomatal-
bearing bryophytes (Chen et al., 2017 and references therein).
Chater et al. (2016) showed that stomatal development in
the moss Physcomitrella patens requires PpSMF1 (SPCH,
MUTE, and FAMA-like) and PpSCRM1, which are the orthologs
of SPCH/MUTE/FAMA and ICE1/SCRM2 in Arabidopsis,
respectively. This suggests that the stomatal development may
be evolutionarily conserved among the land plant lineages. This
hypothesis is further supported by an evolutionary analysis of
relevant proteins among 26 key plant and algae species
(Figure 1B).
Although homologous genes of SMF and ICE/SCRM are mostly
conserved from mosses to angiosperms with stomata, growing
evidence supports the idea that their functions have evolved sub-
stantially (Figure 1C). InP. patens, the cellular process of stomatal
development does not need asymmetric division to produce
a meristemoid cell. Instead, PpSMF1 and PpSCRM1 are
sufficient to initiate stomatal development (Chater et al., 2016).
However, in Arabidopsis, AtSPCH is required to establishativecommons.org/licenses/by/4.0/).
Figure 1. Evolutionary and Developmental
Features for Speedy Grass Stomata.
(A) Images of plants and stomata of Physcomi-
trella patens, Arabidopsis thaliana, and Hordeum
vulgare.
(B) Similarity heatmap for the evolution of sto-
matal development and patterning proteins in
different species. Genesis software was used to
estimate the similarity of proteins. Candidate
protein sequences were selected by BLASTP
searches using Arabidopsis sequences as the
query with the criterion of E value <105. Colored
squares from zero (yellow) to 100% (green) indi-
cate protein sequence similarity in each species
compared with that in Arabidopsis. Gray squares
indicate that no proteins were found that satisfied
the selection criterion.
(C) Models of stomatal development in
P. patens, A. thaliana, and Brachypodium dis-
tachyon. The roles and functions of SPCH,
MUTE, and FAMA-like and ICE/SCRM bHLHs
are divergent in different stages of stomatal
development in moss, Arabidopsis, and Bra-
chypodium. The proteins whose function has
not been thoroughly studied are marked in gray.
ICE1, inducer of CBF expression 1; SCRM2,
scream2; SPCH, speechless; SMF, SPCH,
MUTE, and FAMA-like.
Spotlight Molecular Plantstomatal lineage and drive asymmetric division, and AtMUTE
helps to produce guard mother cells, followed by production
of mature guard cells with AtFAMA (Ohashi-Ito and
Bergmann, 2006; MacAlister et al., 2007; Pillitteri et al., 2007).
The distinct stomatal morphology and patterning between
monocots and dicots may be linked to the gene diversification
and differential protein function. AtICE1 and AtSCRM2 act
redundantly in stomatal development in Arabidopsis, whereas
in B. distachyon, BdICE1 functions in establishing stomatal
fate and BdSCRM2 is essential for differentiation of stomatal
complexes (Raissig et al., 2016). Moreover, the foremost
function of AtSPCH is to drive asymmetric division, but
BdSPCHs were found to determine stomatal fate as BdSPCH2
has the potential in transdifferentiation of hair cells to stomata
(MacAlister et al., 2007; Raissig et al., 2016).
In conclusion, a fundamental evolutionary innovation in
B. distachyon stomatal development appears to be the mobility
of BdMUTE protein, suggesting that BdMUTE might play a vital
role in the formation of subsidiary cells in grasses species
(Raissig et al., 2017). The findings by Raissig et al. (2016, 2017)
and recent advances in the understanding of molecular
evolution of stomatal development show that acquisition of
these novel molecular and evolutionary mechanisms in grass
stomata have resulted in faster and more efficient stomatal
regulation in grass than in many other plant taxa. Utilizing
genes of the bHLH family may well open an important route
toward genetic engineering of major crops with ‘‘superMolecular Plant 10,stomata’’ to improve water use efficiency
and yield. The breakthroughs in genome
editing and other new technologies
provide powerful tools for tackling these
challenges to help meet the need imposed by the global
climate change, booming world population, and declining
arable land for food supply.
FUNDING
Z.-H.C. is supported by the Natural Science Foundation of China (NSFC)
(31620103912, 31571578), a Chinese 1000-Plan project, and an Austra-
lian Research Council (ARC) Discovery Early Career Researcher Award
(DE1401011143). M.R.B. is funded by the UK Biotechnology and Biolog-
ical Sciences Research Council (BBSRC) (BB/K015893/1, BB/N00690/1,
BB/M001601/1, BB/L019205/1, BB/L001276/1) and BBSRC-NSF grant
(BB/M01133X/1).
ACKNOWLEDGMENTS
We thank A/Prof. Fay-wei Li (Cornell University) for the fern gene se-
quences and Qian Yang, Chenchen Zhao, and Guang Chen for their tech-
nical assistance. We apologize to those researchers whose work we have
been unable to cite owing to space limitations. No conflict of interest
declared.
Received: April 25, 2017
Revised: May 23, 2017
Accepted: June 7, 2017
Published: June 14, 2017
Shengguan Cai1,2, Maria Papanatsiou3,
Michael R. Blatt3 and Zhong-Hua Chen1,2,*
1College of Agriculture and Biotechnology, Zhejiang University, Hangzhou
310058, China912–914, July 2017 ª The Author 2017. 913
Molecular Plant Spotlight2School of Science and Health, Hawkesbury Institute for the Environment,
Western Sydney University, Penrith, NSW 2751, Australia
3Laboratory of Plant Physiology and Biophysics, University of Glasgow,
Glasgow G12 8QQ, UK
*Correspondence: Zhong-Hua Chen (z.chen@westernsydney.edu.au)
http://dx.doi.org/10.1016/j.molp.2017.06.002
REFERENCES
Chater, C.C., Caine, R.S., Tomek, M., Wallace, S., Kamisugi, Y.,
Cuming, A.C., Lang, D., MacAlister, C.A., Casson, S., Bergmann,
D.C., et al. (2016). Origin and function of stomata in the moss
Physcomitrella patens. Nat. Plants 2:16179.
Chater, C.C., Caine, R.S., Fleming, A.J., and Gray, J.E. (2017). Origins
and evolution of stomatal development. Plant Physiol. 174:624–638.
Chen, Z.H., Chen, G., Dai, F., Wang, Y., Hills, A., Ruan, Y.L., Zhang, G.,
Franks, P.J., Nevo, E., and Blatt, M.R. (2017). Molecular evolution of
grass stomata. Trends Plant Sci. 22:124–139.
Jezek, M., and Blatt, M.R. (2017). The membrane transport system of the
guard cell and its integration for stomatal dynamics. Plant Physiol.
174:487–519.914 Molecular Plant 10, 912–914, July 2017 ª The Author 2017.MacAlister, C.A., Ohashi-Ito, K., and Bergmann, D.C. (2007).
Transcription factor control of asymmetric cell divisions that establish
the stomatal lineage. Nature 445:537–540.
Ohashi-Ito, K., and Bergmann, D.C. (2006). Arabidopsis FAMA
controls the final proliferation/differentiation switch during stomatal
development. Plant Cell 18:2493–2505.
Pillitteri, L.J., and Torii, K.U. (2012). Mechanisms of stomatal
development. Annu. Rev. Plant Biol. 63:591–614.
Pillitteri, L.J., Sloan, D.B., Bogenschutz, N.L., and Torii, K.U. (2007).
Termination of asymmetric cell division and differentiation of
stomata. Nature 445:501–505.
Raissig, M.T., Abrash, E., Bettadapur, A., Vogel, J.P., and Bergmann,
D.C. (2016). Grasses use an alternatively wired bHLH transcription
factor network to establish stomatal identity. Proc. Natl. Acad. Sci.
USA 113:8326–8331.
Raissig, M.T., Matos, J.L., Gil, X.G., Kornfeld, A., Bettadapur, A.,
Abrash, E., Allison, H.R., Badgley, G., Vogel, J.P., Berry, J.A.,
et al. (2017). Mobile MUTE specifies subsidiary cells to build
physiologically improved grass stomata. Science 355:1215–1218.


Speedy grass stomata: emerging molecular and evolutionary features

Enlighten

Molecular PlantSpotlightSpeedy Grass Stomata: Emerging Molecular andEvolutionary FeaturesPublished by the Molecular Plant Shanghai Editorial Office in association withCell Press, an imprint of Elsevier Inc., on behalf of CSPB and IPPE, SIBS, CAS.Stomata in most land plants are formed by a pair of guard cells,controlling the water loss and the carbon dioxide uptake. Thedevelopment, patterning, and density of stomata are funda-mental traits for stomatal function, contributing to plant growthand productivity (Pillitteri and Torii, 2012). The stomata of mostplant species consist of two kidney-shaped guard cells, whilestomata of grass species are formed by two dumbbell-shapedguard cells flanked by two subsidiary cells (Figure 1A). Thefour-celled stomatal complex in grasses may facilitate a fastresponse to environmental cues for efficient photosynthesisand water use, possibly through the rapid transport of ions andosmolytes between guard cells and subsidiary cells (see Jezekand Blatt, 2017; Chen et al., 2017 and references therein).Given that many grasses are agronomically important speciesas staple food, feed, and biofuel sources, it is vital tounderstand the molecular mechanisms of grass stomatadevelopment and patterning, and of membrane transport inguard cells and subsidiary cells, which govern the opening andclosure of stomatal pores.Our understanding of the genetic control of stomata develop-ment in the model grass species Brachypodium distachyonhas been advanced by two recent groundbreaking studies byRaissig et al. (2016, 2017). The authors investigated the rolesand functions of inducer of CBF expression (ICE)/SCREAM(SCRM) basic helix-loop-helix (bHLH) and SPEECHLESS(SPCH), MUTE, and FAMA-like bHLHs in the model grassB. distachyon by using mutagenesis, genome editing, and otheremerging technologies. Their most exciting discovery is thatBdMUTE acts as one of the key regulators for subsidiary cellformation and proper guard mother cell division. A 5-bp deletionin BdMUTE led to a failure in recruitment of subsidiary cells, andrendered stomata with only two guard cells in the subsidiary cellidentity defective (sid) mutant, which could be complementedby BdMUTEp:BdMUTE. BdMUTE protein was detected inboth guard cells and subsidiary cells, but intriguingly BdMUTEgene is expressed in guard mother cells, suggesting thatBdMUTE protein moves from guard mother cells into subsidiarymother cells, probably via plasmodesmata. The loss of subsid-iary cells in sid could not be rescued by the introduction ofBdMUTEp:AtMUTE, suggesting that mobility is an intrinsicfeature of BdMUTE protein and is essential for subsidiary cellpatterning in grasses. In the model eudicot Arabidopsis, thedevelopment of Arabidopsis stomata depends on group IabHLH transcription factors—AtSPCH, AtMUTE, and AtFAMA—in heterodimeric association with bHLH group IIIb partners,AtICE1 and AtSCRM2 (Pillitteri and Torii, 2012; Chateret al., 2017). Although many key genes regulating stomataldevelopment and patterning have been identified andextensively studied in Arabidopsis (Pillitteri and Torii, 2012;Chater et al., 2017), the discovery of grass-specific function oftheir homologous genes has major implications for plant andagricultural science and evolutionary biology.912 Molecular Plant 10, 912–914, July 2017 ª The Author 2017.This is an open access article under the CC BY license (http://creGrass stomata are unique in nearly all aspects of their physiologyand development compared with non-monocot plant stomata:they show faster stomatal responses, distinct morphologicaland structural features, and unique membrane transport andsignaling systems. We hypothesized that the success of grassis likely attributed to the evolution of highly responsive stomatacapable of maximizing productivity in rapidly changing environ-ments; grass stomata harness the active turgor control mecha-nisms present in stomata of more ancient plant lineages,maximizing several morphological and developmental featuresto ensure rapid responses to environmental inputs (Chen et al.,2017 and references therein). This hypothesis is supportedby the work on subsidiary cell-less sid mutant in Raissiget al. (2017). These authors found that the maximum porearea of stomata in sid mutant was only half of that in the wild-type, even when forced open by the toxin fusicoccin. The sidmutant showed slower stomatal responses to changing lightintensities, and its stomata exhibited a reduced dynamic rangeof apertures compared with the wild-type. Most importantly,the sid mutant produced less biomass than the wild-type,linking BdMUTE-regulated subsidiary cell formation with impacton photosynthesis and biomass production in a grass species.The findings also suggest that engineering the properties of thesubsidiary cell may allow for fine-tuning stomatal responses,which affect photosynthesis, water use efficiency, and cropyield.The early acquisition of stomata is fundamentally important forthe evolution of land plants, and many key genes encoding sto-matal functions have been conserved since the first stomatal-bearing bryophytes (Chen et al., 2017 and references therein).Chater et al. (2016) showed that stomatal development inthe moss Physcomitrella patens requires PpSMF1 (SPCH,MUTE, and FAMA-like) and PpSCRM1, which are the orthologsof SPCH/MUTE/FAMA and ICE1/SCRM2 in Arabidopsis,respectively. This suggests that the stomatal development maybe evolutionarily conserved among the land plant lineages. Thishypothesis is further supported by an evolutionary analysis ofrelevant proteins among 26 key plant and algae species(Figure 1B).Although homologous genes of SMF and ICE/SCRM are mostlyconserved from mosses to angiosperms with stomata, growingevidence supports the idea that their functions have evolved sub-stantially (Figure 1C). InP. patens, the cellular process of stomataldevelopment does not need asymmetric division to producea meristemoid cell. Instead, PpSMF1 and PpSCRM1 aresufficient to initiate stomatal development (Chater et al., 2016).However, in Arabidopsis, AtSPCH is required to establishativecommons.org/licenses/by/4.0/).Figure 1. Evolutionary and DevelopmentalFeatures for Speedy Grass Stomata.(A) Images of plants and stomata of Physcomi-trella patens, Arabidopsis thaliana, and Hordeumvulgare.(B) Similarity heatmap for the evolution of sto-matal development and patterning proteins indifferent species. Genesis software was used toestimate the similarity of proteins. Candidateprotein sequences were selected by BLASTPsearches using Arabidopsis sequences as thequery with the criterion of E value <105. Coloredsquares from zero (yellow) to 100% (green) indi-cate protein sequence similarity in each speciescompared with that in Arabidopsis. Gray squaresindicate that no proteins were found that satisfiedthe selection criterion.(C) Models of stomatal development inP. patens, A. thaliana, and Brachypodium dis-tachyon. The roles and functions of SPCH,MUTE, and FAMA-like and ICE/SCRM bHLHsare divergent in different stages of stomataldevelopment in moss, Arabidopsis, and Bra-chypodium. The proteins whose function hasnot been thoroughly studied are marked in gray.ICE1, inducer of CBF expression 1; SCRM2,scream2; SPCH, speechless; SMF, SPCH,MUTE, and FAMA-like.Spotlight Molecular Plantstomatal lineage and drive asymmetric division, and AtMUTEhelps to produce guard mother cells, followed by productionof mature guard cells with AtFAMA (Ohashi-Ito andBergmann, 2006; MacAlister et al., 2007; Pillitteri et al., 2007).The distinct stomatal morphology and patterning betweenmonocots and dicots may be linked to the gene diversificationand differential protein function. AtICE1 and AtSCRM2 actredundantly in stomatal development in Arabidopsis, whereasin B. distachyon, BdICE1 functions in establishing stomatalfate and BdSCRM2 is essential for differentiation of stomatalcomplexes (Raissig et al., 2016). Moreover, the foremostfunction of AtSPCH is to drive asymmetric division, butBdSPCHs were found to determine stomatal fate as BdSPCH2has the potential in transdifferentiation of hair cells to stomata(MacAlister et al., 2007; Raissig et al., 2016).In conclusion, a fundamental evolutionary innovation inB. distachyon stomatal development appears to be the mobilityof BdMUTE protein, suggesting that BdMUTE might play a vitalrole in the formation of subsidiary cells in grasses species(Raissig et al., 2017). The findings by Raissig et al. (2016, 2017)and recent advances in the understanding of molecularevolution of stomatal development show that acquisition ofthese novel molecular and evolutionary mechanisms in grassstomata have resulted in faster and more efficient stomatalregulation in grass than in many other plant taxa. Utilizinggenes of the bHLH family may well open an important routetoward genetic engineering of major crops with ‘‘superMolecular Plant 10,stomata’’ to improve water use efficiencyand yield. The breakthroughs in genomeediting and other new technologiesprovide powerful tools for tackling thesechallenges to help meet the need imposed by the globalclimate change, booming world population, and decliningarable land for food supply.FUNDINGZ.-H.C. is supported by the Natural Science Foundation of China (NSFC)(31620103912, 31571578), a Chinese 1000-Plan project, and an Austra-lian Research Council (ARC) Discovery Early Career Researcher Award(DE1401011143). M.R.B. is funded by the UK Biotechnology and Biolog-ical Sciences Research Council (BBSRC) (BB/K015893/1, BB/N00690/1,BB/M001601/1, BB/L019205/1, BB/L001276/1) and BBSRC-NSF grant(BB/M01133X/1).ACKNOWLEDGMENTSWe thank A/Prof. Fay-wei Li (Cornell University) for the fern gene se-quences and Qian Yang, Chenchen Zhao, and Guang Chen for their tech-nical assistance. We apologize to those researchers whose work we havebeen unable to cite owing to space limitations. No conflict of interestdeclared.Received: April 25, 2017Revised: May 23, 2017Accepted: June 7, 2017Published: June 14, 2017Shengguan Cai1,2, Maria Papanatsiou3,Michael R. Blatt3 and Zhong-Hua Chen1,2,*1College of Agriculture and Biotechnology, Zhejiang University, Hangzhou310058, China912–914, July 2017 ª The Author 2017. 913Molecular Plant Spotlight2School of Science and Health, Hawkesbury Institute for the Environment,Western Sydney University, Penrith, NSW 2751, Australia3Laboratory of Plant Physiology and Biophysics, University of Glasgow,Glasgow G12 8QQ, UK*Correspondence: Zhong-Hua Chen (z.chen@westernsydney.edu.au)http://dx.doi.org/10.1016/j.molp.2017.06.002REFERENCESChater, C.C., Caine, R.S., Tomek, M., Wallace, S., Kamisugi, Y.,Cuming, A.C., Lang, D., MacAlister, C.A., Casson, S., Bergmann,D.C., et al. (2016). Origin and function of stomata in the mossPhyscomitrella patens. Nat. Plants 2:16179.Chater, C.C., Caine, R.S., Fleming, A.J., and Gray, J.E. (2017). Originsand evolution of stomatal development. Plant Physiol. 174:624–638.Chen, Z.H., Chen, G., Dai, F., Wang, Y., Hills, A., Ruan, Y.L., Zhang, G.,Franks, P.J., Nevo, E., and Blatt, M.R. (2017). Molecular evolution ofgrass stomata. Trends Plant Sci. 22:124–139.Jezek, M., and Blatt, M.R. (2017). The membrane transport system of theguard cell and its integration for stomatal dynamics. Plant Physiol.174:487–519.914 Molecular Plant 10, 912–914, July 2017 ª The Author 2017.MacAlister, C.A., Ohashi-Ito, K., and Bergmann, D.C. (2007).Transcription factor control of asymmetric cell divisions that establishthe stomatal lineage. Nature 445:537–540.Ohashi-Ito, K., and Bergmann, D.C. (2006). Arabidopsis FAMAcontrols the final proliferation/differentiation switch during stomataldevelopment. Plant Cell 18:2493–2505.Pillitteri, L.J., and Torii, K.U. (2012). Mechanisms of stomataldevelopment. Annu. Rev. Plant Biol. 63:591–614.Pillitteri, L.J., Sloan, D.B., Bogenschutz, N.L., and Torii, K.U. (2007).Termination of asymmetric cell division and differentiation ofstomata. Nature 445:501–505.Raissig, M.T., Abrash, E., Bettadapur, A., Vogel, J.P., and Bergmann,D.C. (2016). Grasses use an alternatively wired bHLH transcriptionfactor network to establish stomatal identity. Proc. Natl. Acad. Sci.USA 113:8326–8331.Raissig, M.T., Matos, J.L., Gil, X.G., Kornfeld, A., Bettadapur, A.,Abrash, E., Allison, H.R., Badgley, G., Vogel, J.P., Berry, J.A.,et al. (2017). Mobile MUTE specifies subsidiary cells to buildphysiologically improved grass stomata. Science 355:1215–1218.

Stomata in most land plants are formed by a pair of guard cells, controlling the water loss and the carbon dioxide uptake. The development, patterning, and density of stomata are fundamental traits for stomatal function, contributing to plant growth and productivity (Pillitteri and Torii, 2012). The stomata of most plant species consist of two kidney-shaped guard cells, while stomata of grass species are formed by two dumbbell-shaped guard cells flanked by two subsidiary cells (Figure 1A). The four-celled stomatal complex in grasses may facilitate a fast response to environmental cues for efficient photosynthesis and water use, possibly through the rapid transport of ions and osmolytes between guard cells and subsidiary cells (see Jezek and Blatt, 2017; Chen et al., 2017 and references therein). Given that many grasses are agronomically important species as staple food, feed, and biofuel sources, it is vital to understand the molecular mechanisms of grass stomata development and patterning, and of membrane transport in guard cells and subsidiary cells, which govern the opening and closure of stomatal pores

Speedy grass stomata: emerging molecular and evolutionary features

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