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• W1963893746 abstract "Stomata are pores on the surfaces of leaves that regulate gas exchange between the plant interior and the atmosphere [1Hetherington A.M. Woodward F.I. The role of stomata in sensing and driving environmental change.Nature. 2003; 424: 901-908Crossref PubMed Scopus (1335) Google Scholar]. Plants adapt to changing environmental conditions in the short term by adjusting the aperture of the stomatal pores, whereas longer-term changes are accomplished by altering the proportion of stomata that develop on the leaf surface [2Roelfsema M.R. Hedrich R. In the light of stomatal opening: New insights into ‘the Watergate’.New Phytol. 2005; 167: 665-691Crossref PubMed Scopus (354) Google Scholar, 3Casson S. Gray J.E. Influence of environmental factors on stomatal development.New Phytol. 2008; 178: 9-23Crossref PubMed Scopus (222) Google Scholar]. Although recent work has identified genes involved in the control of stomatal development [4Bergmann D.C. Sack F.D. Stomatal development.Annu. Rev. Plant Biol. 2007; 58: 163-181Crossref PubMed Scopus (287) Google Scholar], we know very little about how stomatal development is modulated by environmental signals, such as light. Here, we show that mature leaves of Arabidopsis grown at higher photon irradiances show significant increases in stomatal index (S.I.) [5Salisbury E.J. On the causes and ecological significance of stomatal frequency, with special reference to the woodland flora.Philosophical Transactions of the Royal Society of London. 1928; 216B: 1-65Crossref Google Scholar] compared to those grown at lower photon irradiances. Light quantity-mediated changes in S.I. occur in red light, suggesting that phytochrome photoreceptors [6Franklin K.A. Whitelam G.C. Phytochromes and shade-avoidance responses in plants.Ann. Bot. (Lond.). 2005; 96: 169-175Crossref PubMed Scopus (335) Google Scholar] are involved. By using a genetic approach, we demonstrate that this response is dominated by phytochrome B and also identify a role for the transcription factor, PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) [7Huq E. Quail P.H. PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis.EMBO J. 2002; 21: 2441-2450Crossref PubMed Scopus (366) Google Scholar]. In sum, we identify a photoreceptor and downstream signaling protein involved in light-mediated control of stomatal development, thereby establishing a tractable system for investigating how an environmental signal modulates stomatal development. Stomata are pores on the surfaces of leaves that regulate gas exchange between the plant interior and the atmosphere [1Hetherington A.M. Woodward F.I. The role of stomata in sensing and driving environmental change.Nature. 2003; 424: 901-908Crossref PubMed Scopus (1335) Google Scholar]. Plants adapt to changing environmental conditions in the short term by adjusting the aperture of the stomatal pores, whereas longer-term changes are accomplished by altering the proportion of stomata that develop on the leaf surface [2Roelfsema M.R. Hedrich R. In the light of stomatal opening: New insights into ‘the Watergate’.New Phytol. 2005; 167: 665-691Crossref PubMed Scopus (354) Google Scholar, 3Casson S. Gray J.E. Influence of environmental factors on stomatal development.New Phytol. 2008; 178: 9-23Crossref PubMed Scopus (222) Google Scholar]. Although recent work has identified genes involved in the control of stomatal development [4Bergmann D.C. Sack F.D. Stomatal development.Annu. Rev. Plant Biol. 2007; 58: 163-181Crossref PubMed Scopus (287) Google Scholar], we know very little about how stomatal development is modulated by environmental signals, such as light. Here, we show that mature leaves of Arabidopsis grown at higher photon irradiances show significant increases in stomatal index (S.I.) [5Salisbury E.J. On the causes and ecological significance of stomatal frequency, with special reference to the woodland flora.Philosophical Transactions of the Royal Society of London. 1928; 216B: 1-65Crossref Google Scholar] compared to those grown at lower photon irradiances. Light quantity-mediated changes in S.I. occur in red light, suggesting that phytochrome photoreceptors [6Franklin K.A. Whitelam G.C. Phytochromes and shade-avoidance responses in plants.Ann. Bot. (Lond.). 2005; 96: 169-175Crossref PubMed Scopus (335) Google Scholar] are involved. By using a genetic approach, we demonstrate that this response is dominated by phytochrome B and also identify a role for the transcription factor, PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) [7Huq E. Quail P.H. PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis.EMBO J. 2002; 21: 2441-2450Crossref PubMed Scopus (366) Google Scholar]. In sum, we identify a photoreceptor and downstream signaling protein involved in light-mediated control of stomatal development, thereby establishing a tractable system for investigating how an environmental signal modulates stomatal development. Light is one of the most important signals controlling plant development [8Chen M. Chory J. Fankhauser C. Light signal transduction in higher plants.Annu. Rev. Genet. 2004; 38: 87-117Crossref PubMed Scopus (661) Google Scholar]. For example, increased photon irradiance results in significant increases in stomatal index (S.I., the ratio of the number of stomata in a given area divided by the total number of stomata and other epidermal cells in that same area) [9Ticha I. Photosynthetic characteristics during ontogenesis of leaves. 7. Stomata density and sizes.Photosynthetica. 1982; 16: 375-471Google Scholar, 10Lake J.A. Quick W.P. Beerling D.J. Woodward F.I. Plant development. Signals from mature to new leaves.Nature. 2001; 411: 154Crossref PubMed Scopus (297) Google Scholar], indicating that light influences stomatal development. To investigate the molecular basis of this response, we first established that stomatal indices in Arabidopsis accessions Col-0 and Ws were higher in plants grown at 175 μmol m−2 s−1 compared with plants grown at 50 μmol m−2 s−1 white light (Figure 1A). In both accessions, plants grown at 175 μmol m−2 s−1 had stomatal and epidermal cell densities higher than those observed at 50 μmol m−2 s−1 (Figure S1A available online). The increase in stomatal index between plants grown at these photon irradiances must, therefore, be due to a proportionally greater increase in stomatal numbers, and, hence, it can be concluded that light signals positively influence stomatal fate. It should be noted that, in these and all subsequent experiments, stomatal spacing was not affected, and no clustering was observed. We hypothesized that this change in the developmental program of leaf epidermal cells in response to light quantity could be mediated by plant photoreceptors. These belong to three main families: the red and far-red light-sensing phytochromes and the blue and UV-A light-sensing cryptochromes and phototropins [11Franklin K.A. Larner V.S. Whitelam G.C. The signal transducing photoreceptors of plants.Int. J. Dev. Biol. 2005; 49: 653-664Crossref PubMed Scopus (137) Google Scholar]. To investigate whether phytochromes were involved in the light-mediated control of stomatal development, we measured the stomatal index of plants grown under different photon irradiances of monochromatic red light (conditions in which only the phytochromes and not other plant photoreceptors are active). We showed that the stomatal index of plants grown under the higher photon irradiances of red light was significantly higher than that grown at the lower irradiance (Col-0 p value = 3.5 × 10−5; Ws p value = 2.2 × 10−3) (Figure 1B). For the Ws accession, the cell density data mimicked the results observed in white light, whereas, in Col-0, only stomatal density increased significantly at the higher photon irradiance of red light, suggesting accession-specific differences in cell division activity in the different light regimes, which may include a differential response between the two accessions to blue light (Figure S1B). Taken together, these results indicate that the phytochromes have a role to play in mediating changes in stomatal development in response to changes in light quantity. In Arabidopsis, there are five members of the phytochrome gene family (PHYA to PHYE) [12Clack T. Mathews S. Sharrock R.A. The phytochrome apoprotein family in Arabidopsis is encoded by five genes: The sequences and expression of PHYD and PHYE.Plant Mol. Biol. 1994; 25: 413-427Crossref PubMed Scopus (540) Google Scholar]. To investigate which member or members are involved in the regulation of stomatal development, we measured stomatal indices in mutants defective in the separate phytochrome genes. We did not investigate stomatal development in phyE mutants. This is because the only available alleles of this gene are in the Ler accession [13Devlin P.F. Patel S.R. Whitelam G.C. Phytochrome E influences internode elongation and flowering time in Arabidopsis.Plant Cell. 1998; 10: 1479-1487PubMed Google Scholar]. Given that the ERECTA gene encodes a putative leucine-rich receptor and erecta mutants are characterized by, among other abnormalities, alterations to stomatal density and leaf morphology compared with the appropriate control [14Shpak E.D. McAbee J.M. Pillitteri L.J. Torii K.U. Stomatal patterning and differentiation by synergistic interactions of receptor kinases.Science. 2005; 309: 290-293Crossref PubMed Scopus (404) Google Scholar, 15Masle J. Gilmore S.R. Farquhar G.D. The ERECTA gene regulates plant transpiration efficiency in Arabidopsis.Nature. 2005; 436: 866-870Crossref PubMed Scopus (419) Google Scholar], we felt it was inappropriate to work on this material. In addition, S.I. in the Ler accession (15.2% at 175 μmol m−2 s−1) was significantly lower than Col-0 or Ws under all photon irradiances. Furthermore, it did not show a robust response between the different photon irradiances, suggesting that the er mutation (or other accession-specific factors) may be dominant to the light quantity signal. When grown in white light at 175 μmol m−2 s−1 or 50 μmol m−2 s−1, neither single mutants in phyA and phyC nor a phyAC double mutant showed any significant difference in stomatal index compared with the Col-0 wild-type (also see below). By way of contrast, at the higher photon irradiance, plants defective in phyB, either as the single mutant or the phyBC and phyAB double mutants (phyAB p value = 0.001; data not shown), showed a significant reduction in stomatal index compared with the Col-0 wild-type. Consistent with the suggestion that phyB, but not phyA or phyC, contributes significantly to the control of stomatal development, at the photon irradiances used in these experiments, we found that stomatal indices in the phyBC double mutants (and phyAB; data not shown) were not significantly different than those in the phyB single mutant (Figure 2A). To investigate whether phyD has a role to play in this response, we examined the stomatal index of the Arabidopsis Ws accession, which is naturally defective in phyD [16Aukerman M.J. Hirschfeld M. Wester L. Weaver M. Clack T. Amasino R.M. Sharrock R.A. A deletion in the PHYD gene of the Arabidopsis Wassilewskija ecotype defines a role for phytochrome D in red/far-red light sensing.Plant Cell. 1997; 9: 1317-1326PubMed Google Scholar]. An introgressed PHYD line ([16Aukerman M.J. Hirschfeld M. Wester L. Weaver M. Clack T. Amasino R.M. Sharrock R.A. A deletion in the PHYD gene of the Arabidopsis Wassilewskija ecotype defines a role for phytochrome D in red/far-red light sensing.Plant Cell. 1997; 9: 1317-1326PubMed Google Scholar]; Figure 2B, Ws+D) did not show a significant difference to the Ws control, indicating that, as with phyA and phyC mutants in Col-0, phyD does not appear to contribute significantly to this response under these conditions. Furthermore, no significant change in stomatal index was observed in phyAD/CD/ACD mutants (accession Ws), indicating that these family members are not acting redundantly in this response. This is significant given that, in Col-0, the stomatal index of phyAC mutant is reduced, but not significantly, compared with the control. Therefore, by examining both accessions, we conclude that phyA and phyC are unlikely to be acting in concert to redundantly regulate this response. However, as was observed in Col-0, mutants defective in phyB (phyBD and phyBCD, p values = 7.0 × 10−4 and 8.9 × 10−4, respectively) did show a significant reduction in stomatal index when grown in white light at 175 μmol m−2 s−1, verifying the requirement for phyB in mediating this response. Interestingly, unlike Col-0, phyB mutants in the Ws accession also showed significantly reduced stomatal indices at the lower photon irradiance, suggesting that other accession-specific factors may control the sensitivity of this response to light quantity. In the Ws accession, it is apparent that the reduction in stomatal indices observed in genotypes defective in phyB is due to increases in epidermal cell number because stomatal density is relatively stable (Figures S2C and S2D). This is not so evident in the Col-0 accession in which the general trend was for reduced stomatal and epidermal cell densities in all phytochrome mutants grown at 175 μmol m−2 s−1 compared with the wild-type control (Figures S2A and S2B). The reduced stomatal indices of the phyB mutant genotypes at 175 μmol m−2 s−1 compared with those of the Col-0 wild-type is, therefore, likely to be due to either a proportionally smaller light-induced increase in stomatal number or a proportionally greater light-induced increase in epidermal cell number in phyB mutant genotypes—or due to both of these possibilities operating in parallel. What is evident is that, whereas the phytochrome mutants in the two accessions show different cell density responses, the common output is a reduction in stomatal index in phyB mutant genotypes. From these results and those from the plants grown in monochromatic red light, it is possible to conclude that light quantity-induced changes in stomatal index and, therefore, stomatal development are mediated, at least in part, by the phytochrome family of photoreceptors, with phyB assuming the dominant role. Whereas mutations in PHYA, PHYC, and PHYD do have effects on cell density, significant changes in stomatal index are not observed, and, therefore, they do not appear to contribute significantly under these conditions, although it is possible that they work redundantly in combination with phyE, which was not tested in this study. Following photoactivation, phyB has been shown to translocate from the cytoplasm to the nucleus [17Sakamoto K. Nagatani A. Nuclear localization activity of phytochrome B.Plant J. 1996; 10: 859-868Crossref PubMed Scopus (226) Google Scholar, 18Yamaguchi R. Nakamura M. Mochizuki N. Kay S.A. Nagatani A. Light-dependent translocation of a phytochrome B-GFP fusion protein to the nucleus in transgenic Arabidopsis.J. Cell Biol. 1999; 145: 437-445Crossref PubMed Scopus (284) Google Scholar], a step that is crucial with respect to phyB function [19Huq E. Al-Sady B. Quail P.H. Nuclear translocation of the photoreceptor phytochrome B is necessary for its biological function in seedling photomorphogenesis.Plant J. 2003; 35: 660-664Crossref PubMed Scopus (97) Google Scholar]. Within the nucleus, active phytochromes have been shown to interact with the phytochrome-interacting factors (PIFs), which consist of several closely related bHLH transcription factors [20Monte E. Al-Sady B. Leivar P. Quail P.H. Out of the dark: How the PIFs are unmasking a dual temporal mechanism of phytochrome signalling.J. Exp. Bot. 2007; 58: 3125-3133Crossref PubMed Scopus (57) Google Scholar]. Several studies have now confirmed mechanisms and regulatory roles for PIFs in regulating phytochrome signaling [7Huq E. Quail P.H. PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis.EMBO J. 2002; 21: 2441-2450Crossref PubMed Scopus (366) Google Scholar, 21Al-Sady B. Kikis E.A. Monte E. Quail P.H. Mechanistic duality of transcription factor function in phytochrome signaling.Proc. Natl. Acad. Sci. USA. 2008; 105: 2232-2237Crossref PubMed Scopus (87) Google Scholar, 22Al-Sady B. Ni W. Kircher S. Schafer E. Quail P.H. Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation.Mol. Cell. 2006; 23: 439-446Abstract Full Text Full Text PDF PubMed Scopus (347) Google Scholar, 23Leivar P. Monte E. Al-Sady B. Carle C. Storer A. Alonso J.M. Ecker J.R. Quail P.H. The Arabidopsis phytochrome-interacting factor PIF7, together with PIF3 and PIF4, regulates responses to prolonged red light by modulating phyB levels.Plant Cell. 2008; 20: 337-352Crossref PubMed Scopus (237) Google Scholar, 24Monte E. Tepperman J.M. Al-Sady B. Kaczorowski K.A. Alonso J.M. Ecker J.R. Li X. Zhang Y. Quail P.H. The phytochrome-interacting transcription factor, PIF3, acts early, selectively, and positively in light-induced chloroplast development.Proc. Natl. Acad. Sci. USA. 2004; 101: 16091-16098Crossref PubMed Scopus (225) Google Scholar, 25de Lucas M. Daviere J.M. Rodriguez-Falcon M. Pontin M. Iglesias-Pedraz J.M. Lorrain S. Fankhauser C. Blazquez M.A. Titarenko E. Prat S. A molecular framework for light and gibberellin control of cell elongation.Nature. 2008; 451: 480-484Crossref PubMed Scopus (785) Google Scholar, 26Lorrain S. Allen T. Duek P.D. Whitelam G.C. Fankhauser C. Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors.Plant J. 2008; 53: 312-323Crossref PubMed Scopus (463) Google Scholar, 27Feng S. Martinez C. Gusmaroli G. Wang Y. Zhou J. Wang F. Chen L. Yu L. Iglesias-Pedraz J.M. Kircher S. et al.Coordinated regulation of Arabidopsis thaliana development by light and gibberellins.Nature. 2008; 451: 475-479Crossref PubMed Scopus (689) Google Scholar]. Given their role in phytochrome signaling, we used mutants defective in PIF3, PIF4, PIF5, and PIF6 to assess whether these PIFs mediate changes in stomatal index in response to light. The stomatal indices of pif3, pif5, and pif6 mutants were not significantly different from those of the wild-type (Col-0) at the higher photon irradiance. By contrast, when grown at the higher irradiance and in comparison to Col-0, pif4 (p value = 3.5 × 10−3) and a pif4 pif5 double mutant (p value = 0.041) showed significantly reduced stomatal indices (Figure 3A), as well as reduced stomatal densities (Figures S3A and S3B), consistent with a role for PIF4 in the control of this response. In addition, because there was no additive effect evident in pif4 pif5 plants with regards to their stomatal index, we conclude that PIF5 does not contribute to the control of stomatal development under the growth conditions that we have used (Figure 3A). As with the phytochrome mutants in the Col-0 accession, no significant difference in stomatal index was found in plants grown at the lower photon irradiance, except for pif6 leaves, which showed an increase in stomatal index (Figure 3A). Although it was not investigated further, this latter result might indicate that, in the control of stomatal development by light, individual PIFs may have photon irradiance-specific effects. To confirm the role of PIF4 in regulating stomatal development in response to changes in light quantity and to determine whether this response was dependent on phytochrome signaling, we grew pif4 plants under red light at 130 μmol m−2 s−1 (leaf development was too retarded in these mutants at lower photon irradiances to enable analysis). Under these conditions, phyB mutants in the Arabidopsis accessions Col-0 and Ws both showed significantly reduced stomatal indices compared with those of their respective controls (Col-0 p value = 1.1 × 10−5; Ws p value = 6.9 × 10−6), confirming the dominant role of this photoreceptor in this response (Figure 3B). pif4 mutants also showed an attenuated response in red light (p value 5.6 × 10−3), whereas pif5 mutants were indistinguishable from the Col-0 control (Figure 3B). These data confirm that PIF4 is required for light quantity-mediated changes in stomatal development. We then asked whether this response is dependent on phyB activity or whether PIF4 mediates this response in conjunction with other members of the phytochrome gene family. The response of a phyB pif4 double mutant was examined and compared with both phyB and pif4 mutants (see Figure S5 for plant phenotypes and impressions). As was observed previously in both white and red light, both of the single mutants had significantly reduced stomatal indices at the higher photon irradiance (175 μmol m−2 s−1; phyB p value = 3.1 × 10−6; pif4 p value = 0.010). The phyB pif4 mutant was found to be virtually indistinguishable from the phyB single mutant (Figure 3C; data not shown) (p value 2.2 × 10−8). The response of the phyB mutant is significantly different from that of the pif4 mutant, which suggests that phyB may also influence this response via a PIF4-independent pathway. Consistent with our previous findings, at the lower photon irradiance (50 μmol m−2 s−1), no significant differences were observed between the mutant genotypes and the Col-0 wild-type (data not shown). Therefore, both phyB and pif4 mutants show attenuated responses to the higher photon irradiances used in this study (Figures 2, 3A–3C, and S4). It should be noted that plants deficient in phyB and PIF4 do not show a complete inhibition of the response to changes in light quantity. Other factors may, therefore, act either in concert or in parallel to mediate this response, with phyB and PIF4 assuming dominant roles. In conclusion, these data are, therefore, consistent with PIF4 acting in a phyB-dependent manner to modulate stomatal development in response to light signals. The abaxial epidermal surface of Arabidopsis rosette leaves consists mostly of either stomata or epidermal cells, predominantly tessellated pavement cells in the fully differentiated epidermis. Plants grown at the higher photon irradiances of both white and red light used in this study show significant increases in stomatal index, indicating that epidermal cell-fate decisions are influenced by light quantity signals. At increased photon irradiances, light is likely to regulate stomatal index through positive influences on stomatal fate, negative effects on pavement cell fate, or by controlling these two processes in parallel; whatever the mechanism, the net result is the same—an increase in stomatal index. The cell density data for the Arabidopsis accessions used in this study, Col-0 and Ws, indicate that both accessions respond similarly to white light but differently to red light (Figures S1A and S1B), whereas the stomatal index response is consistent between the accessions and the light regimes. We have only analyzed the mature leaf phenotypes for these two accessions. From these data, it is not possible to determine that the developmental pathways by which these accessions respond to light are the same. However, from analysis of the phytochrome and pif mutants (Figure 2, Figure 3, S2, and S3), it is evident that cell-fate decisions in the epidermis are not simply correlated with changes in stomatal or epidermal cell density. This is particularly evident when considering the phytochrome mutants. For example, in the Col-0 accession, phyA mutants show reduced cell densities (both of stomata and epidermal cells) at both 175 and 50 μmol m−2 s−1, whereas this is not the case in phyAD mutants in the Ws accession (compared with Ws [phyD]) (Figures S2A–S2D). Significantly, in both Col-0 and Ws, phyA genotypes do not show differences in stomatal index compared with their respective wild-type controls. Also, both the pif4 and pif5 mutants show reductions in cell density at both of the photon irradiances used in this study, yet only pif4 mutants show a significantly reduced stomatal index (at 175 μmol m−2 s−1). These data indicate that the control of the proportion of cells in the epidermis that are guard cells (stomatal index) may be distinguishable in signaling terms from the pathway(s) that controls the final number of cells that form per unit area (density), though further experimentation will be required to examine this possibility. The consequences, in terms of plant physiology and fitness, remain to be determined. Stomatal development is regulated at multiple levels [3Casson S. Gray J.E. Influence of environmental factors on stomatal development.New Phytol. 2008; 178: 9-23Crossref PubMed Scopus (222) Google Scholar, 4Bergmann D.C. Sack F.D. Stomatal development.Annu. Rev. Plant Biol. 2007; 58: 163-181Crossref PubMed Scopus (287) Google Scholar]. The initiation process and the spacing of divisions are controlled by a presumed peptide-based signaling pathway involving the peptide product of the EPIDERMAL PATTERNING FACTOR 1 (EPF1) gene [28Hara K. Kajita R. Torii K.U. Bergmann D.C. Kakimoto T. The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule.Genes Dev. 2007; 21: 1720-1725Crossref PubMed Scopus (323) Google Scholar] and an independent pathway involving STOMATAL DISTRIBUTION AND DENSITY 1 (SDD1, encoding a putative subtilisin-like protease) [29Berger D. Altmann T. A subtilisin-like serine protease involved in the regulation of stomatal density and distribution in Arabidopsis thaliana.Genes Dev. 2000; 14: 1119-1131PubMed Google Scholar]. Several members of the bHLH transcription factor family have been shown to regulate stomatal development [30Ohashi-Ito K. Bergmann D.C. Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development.Plant Cell. 2006; 18: 2493-2505Crossref PubMed Scopus (285) Google Scholar, 31MacAlister C.A. Ohashi-Ito K. Bergmann D.C. Transcription factor control of asymmetric cell divisions that establish the stomatal lineage.Nature. 2007; 445: 537-540Crossref PubMed Scopus (337) Google Scholar, 32Pillitteri L.J. Sloan D.B. Bogenschutz N.L. Torii K.U. Termination of asymmetric cell division and differentiation of stomata.Nature. 2007; 445: 501-505Crossref PubMed Scopus (301) Google Scholar, 33Kanaoka M.M. Pillitteri L.J. Fujii H. Yoshida Y. Bogenschutz N.L. Takabayashi J. Zhu J.K. Torii K.U. SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to Arabidopsis stomatal differentiation.Plant Cell. 2008; 20: 1775-1785Crossref PubMed Scopus (311) Google Scholar]. The closely related bHLH transcription factors SPEECHLESS (SPCH), MUTE, and FAMA have been shown to regulate consecutive steps in the differentiation pathway of stomata [30Ohashi-Ito K. Bergmann D.C. Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development.Plant Cell. 2006; 18: 2493-2505Crossref PubMed Scopus (285) Google Scholar, 31MacAlister C.A. Ohashi-Ito K. Bergmann D.C. Transcription factor control of asymmetric cell divisions that establish the stomatal lineage.Nature. 2007; 445: 537-540Crossref PubMed Scopus (337) Google Scholar, 32Pillitteri L.J. Sloan D.B. Bogenschutz N.L. Torii K.U. Termination of asymmetric cell division and differentiation of stomata.Nature. 2007; 445: 501-505Crossref PubMed Scopus (301) Google Scholar]. Two more distantly related bHLH transcription factors, ICE1/SCREAM and SCREAM2, are also required to initiate the stomatal lineage and, through interactions with SPCH, MUTE, and FAMA, are believed to modulate progression through the consecutive stages of stomatal development [33Kanaoka M.M. Pillitteri L.J. Fujii H. Yoshida Y. Bogenschutz N.L. Takabayashi J. Zhu J.K. Torii K.U. SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to Arabidopsis stomatal differentiation.Plant Cell. 2008; 20: 1775-1785Crossref PubMed Scopus (311) Google Scholar]. Entry into the stomatal developmental pathway is, in part, mediated by the leucine-rich repeat receptor-like protein TOO MANY MOUTHS (TMM) [34Nadeau J.A. Sack F.D. Control of stomatal distribution on the Arabidopsis leaf surface.Science. 2002; 296: 1697-1700Crossref PubMed Scopus (366) Google Scholar], which is believed to form an active complex at the cell surface with members of the ERECTA family of LRR-RLK [14Shpak E.D. McAbee J.M. Pillitteri L.J. Torii K.U. Stomatal patterning and differentiation by synergistic interactions of receptor kinases.Science. 2005; 309: 290-293Crossref PubMed Scopus (404) Google Scholar]. This putative complex is then believed to signal through a MAP kinase signaling pathway, headed by the putative MAP kinase kinase kinase YODA [35Bergmann D.C. Lukowitz W. Somerville C.R. Stomatal development and pattern controlled by a MAPKK kinase.Science. 2004; 304: 1494-1497Crossref PubMed Scopus (401) Google Scholar], to negatively regulate stomatal development by an as yet undetermined mechanism, potentially by targeting the bHLH transcription factors that positively mediate the steps in stomatal differentiation. Photoactivated phyB and PIF4 are both nuclear factors [7Huq E. Quail P.H. PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis.EMBO J. 2002; 21: 2441-2450Crossref PubMed Scopus (366) Google Scholar, 19Huq E. Al-Sady B. Quail P.H. Nuclear translocation of the photoreceptor phytochrome B is necessary for its biological function in seedling photomorphogenesis.Plant J. 2003; 35: 660-664Crossref PubMed Scopus (97) Google Scholar] and are, therefore, less likely to interact with cell-surface receptors. In considering possible mechanisms of action, it is interesting to note that the bHLH transcription factors ICE1/SCM and SCM2 are able to interact with SPCH, MUTE, and FAMA, interactions that presumably influence the activity of these bHLH heterodimers [33Kanaoka M.M. Pillitteri L.J. Fujii H. Yoshida Y. Bogenschutz N.L. Takabayashi J. Zhu J.K. Torii K.U. SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to Arabidopsis stomatal differentiation.Plant Cell. 2008; 20: 1775-1785Crossref PubMed Scopus (311) Google Scholar]. It is possible, therefore, that, as a member of the bHLH family, PIF4 may influence the activity of the stomatal developmental pathway by interactions with these core factors, with phyB influencing the stability of these interactions via its interactions with PIF4. It has been shown that the response to light quantity, as well as to changes in carbon dioxide concentration, is mediated by mature leaves signaling to the developing leaf primordia [10Lake J.A. Quick W.P. Beerling D.J. Woodward F.I. Plant development. Signals from mature to new leaves.Nature. 2001; 411: 154Crossref PubMed Scopus (297) Google Scholar, 36Coupe S.A. Palmer B.G. Lake J.A. Overy S.A. Oxborough K. Woodward F.I. Gray J.E. Quick W.P. Systemic signalling of environmental cues in Arabidopsis leaves.J. Exp. Bot. 2006; 57: 329-341Crossref PubMed Scopus (123) Google Scholar]. Although this systemic signaling response was not investigated in this study, it seems that phyB is most likely to be necessary at the site of signal perception—the mature leaves—and, therefore, may be a component of the signaling pathway responsible for the generation of a putative systemic signal, though a role for phyB locally cannot be discounted. PIF4 may act either in the mature leaves downstream of phyB in the generation of such a signal, in the developing leaf primordia by potentially interacting with the stomatal pathway, or both locally and systemically to regulate the response to light quantity. It is unusual that, in this study, phyB and PIF4 both display positive roles in regulating stomatal development in response to light quantity, given that previous research has shown that PIF4 negatively regulates phyB signaling [7Huq E. Quail P.H. PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis.EMBO J. 2002; 21: 2441-2450Crossref PubMed Scopus (366) Google Scholar, 23Leivar P. Monte E. Al-Sady B. Carle C. Storer A. Alonso J.M. Ecker J.R. Quail P.H. The Arabidopsis phytochrome-interacting factor PIF7, together with PIF3 and PIF4, regulates responses to prolonged red light by modulating phyB levels.Plant Cell. 2008; 20: 337-352Crossref PubMed Scopus (237) Google Scholar, 25de Lucas M. Daviere J.M. Rodriguez-Falcon M. Pontin M. Iglesias-Pedraz J.M. Lorrain S. Fankhauser C. Blazquez M.A. Titarenko E. Prat S. A molecular framework for light and gibberellin control of cell elongation.Nature. 2008; 451: 480-484Crossref PubMed Scopus (785) Google Scholar, 26Lorrain S. Allen T. Duek P.D. Whitelam G.C. Fankhauser C. Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors.Plant J. 2008; 53: 312-323Crossref PubMed Scopus (463) Google Scholar]. These studies have dealt with responses that typically focus on cell elongation rather than cellular differentiation as is the case here. Similar observations have been made for PIF3, which has been shown to be both a positive and negative regulator of different aspects of phytochrome signaling [24Monte E. Tepperman J.M. Al-Sady B. Kaczorowski K.A. Alonso J.M. Ecker J.R. Li X. Zhang Y. Quail P.H. The phytochrome-interacting transcription factor, PIF3, acts early, selectively, and positively in light-induced chloroplast development.Proc. Natl. Acad. Sci. USA. 2004; 101: 16091-16098Crossref PubMed Scopus (225) Google Scholar, 37Bauer D. Viczian A. Kircher S. Nobis T. Nitschke R. Kunkel T. Panigrahi K.C. Adam E. Fejes E. Schafer E. et al.Constitutive photomorphogenesis 1 and multiple photoreceptors control degradation of phytochrome interacting factor 3, a transcription factor required for light signaling in Arabidopsis.Plant Cell. 2004; 16: 1433-1445Crossref PubMed Scopus (321) Google Scholar, 38Kim J. Yi H. Choi G. Shin B. Song P.S. Choi G. Functional characterization of phytochrome interacting factor 3 in phytochrome-mediated light signal transduction.Plant Cell. 2003; 15: 2399-2407Crossref PubMed Scopus (231) Google Scholar]. It is clear that an understanding of the mechanisms involved in this response will require significant further experimentation. To date, the only gene known to be involved in the control of stomatal development in response to environmental signals is the HIGH CARBON DIOXIDE (HIC) gene, which, by an unknown mechanism, regulates stomatal development in plants grown at elevated levels of carbon dioxide [39Gray J.E. Holroyd G.H. van der Lee F.M. Bahrami A.R. Sijmons P.C. Woodward F.I. Schuch W. Hetherington A.M. The HIC signalling pathway links CO2 perception to stomatal development.Nature. 2000; 408: 713-716Crossref PubMed Scopus (15) Google Scholar]. Here, we provide evidence that a specific photoreceptor (phyB) and a putative transcription factor (PIF4) known to be involved in phytochrome signaling are required in the increased photon irradiance-mediated control of epidermal cell-fate decisions in stomatal development. Not only does this work establish a region of the light spectrum responsible for controlling stomatal development together with the photoreceptor and a putative transcription factor involved in the pathway, but it also provides a tractable system for investigating how pathways from environmental signals interact with the basal pathway responsible for the control of stomatal development. phytochrome mutant alleles for the Col-0 accession of Arabidopsis thaliana were phyA-211 and phyB-9. phyC, phyAC, and phyBC have been described [40Monte E. Alonso J.M. Ecker J.R. Zhang Y. Li X. Young J. Austin-Phillips S. Quail P.H. Isolation and characterization of phyC mutants in Arabidopsis reveals complex crosstalk between phytochrome signaling pathways.Plant Cell. 2003; 15: 1962-1980Crossref PubMed Scopus (153) Google Scholar]. phytochrome mutants in the Ws accession have been previously described [41Franklin K.A. Davis S.J. Stoddart W.M. Vierstra R.D. Whitelam G.C. Mutant analyses define multiple roles for phytochrome C in Arabidopsis photomorphogenesis.Plant Cell. 2003; 15: 1981-1989Crossref PubMed Scopus (117) Google Scholar]. pif4, pif5, pif4 pif5, and phyB pif4 mutants have been previously described [26Lorrain S. Allen T. Duek P.D. Whitelam G.C. Fankhauser C. Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors.Plant J. 2008; 53: 312-323Crossref PubMed Scopus (463) Google Scholar], as has pif3-1 [24Monte E. Tepperman J.M. Al-Sady B. Kaczorowski K.A. Alonso J.M. Ecker J.R. Li X. Zhang Y. Quail P.H. The phytochrome-interacting transcription factor, PIF3, acts early, selectively, and positively in light-induced chloroplast development.Proc. Natl. Acad. Sci. USA. 2004; 101: 16091-16098Crossref PubMed Scopus (225) Google Scholar]. A T-DNA insertion in the first exon of the PIF6 gene (SALK_090239c) was obtained from the Nottingham Arabidopsis Stock Centre, and homozygous plants were verified by PCR and sequencing. Arabidopsis plants were grown in growth chambers (Snijder Microclima 1000E, Snijder Scientific, The Netherlands) from seed in 3:1 mix of compost-horticultural silver sand in short days (10 hr photoperiod, 70% RH, 22°C) at photon irradiances of either 175 or 50 μmol m−2 s−1 supplied by fluorescent light (Brite Gro and T5). For monochromatic red light experiments, densely packed light-emitting diodes provided light at λmax 665 nm [42Franklin K.A. Allen T. Whitelam G.C. Phytochrome A is an irradiance-dependent red light sensor.Plant J. 2007; 50: 108-117Crossref PubMed Scopus (59) Google Scholar] at either 130 or 65μmol m−2 s−1, filtered through 20 mm water to remove radiant heating (18 hr photoperiod, 22°C). Impressions of the abaxial surface of mature rosette leaves, principal growth stage 5.10 [43Boyes D.C. Zayed A.M. Ascenzi R. McCaskill A.J. Hoffman N.E. Davis K.R. Gorlach J. Growth stage-based phenotypic analysis of Arabidopsis: A model for high throughput functional genomics in plants.Plant Cell. 2001; 13: 1499-1510PubMed Google Scholar], were made with dental resin (President Jet Light Body, Coltène/Whaledent, Burgess Hill, UK). Clear nail varnish was applied to the set impression after removal from the leaf, and the varnish impressions were viewed on a Zeiss Axiovert 200M inverted microscope and imaged with Volocity software (Improvision Ltd, Coventry, UK). Stomatal and epidermal cell counts were taken from three areas per leaf with three leaves per plant from four separate plants, for a total of 36 measurements. For the density data, the mean was calculated from the total number of stomata or epidermal cells. The stomatal index was calculated for each area individually, and the mean was then calculated from these data. Stomatal index was calculated with the following formula: S.I. = [number of stomata/(number of other epidermal cells + number of stomata)] × 100. For statistical analysis, an unpaired t test was performed on the data following arcsine transformation, which was performed because stomatal index is a proportion and not a direct measurement. Leaf area data are provided in Figure S6. This paper is dedicated to Garry Whitelam, who died during the course of the final revisions to this manuscript. He was a generous and inspirational colleague who has left a lasting impression on international photobiological research. He will be greatly missed. phyC, phyAC, and phyBC seed was kindly supplied by Peter Quail (University of California, Berkeley). pif4, pif5, pif4 pif5, and phyB pif4 seed was kindly supplied by Christian Fankhauser (University of Lausanne). S.A.C., A.M.H., and C.S.G. acknowledge the support of the Leverhulme Trust. Download .pdf (.85 MB) Help with pdf files Document S1. Six Figures" @default.
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• W1963893746 title "phytochrome B and PIF4 Regulate Stomatal Development in Response to Light Quantity" @default.
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