- Email: [email protected]
Animal Navigation: Birds Have Magnetic Maps
Current Biology
Dispatches cilia shapes and sizes. How is the regional ciliary length pattern of the olfactory epithelium established and maintained? Challis et al. [1] have ruled out a role for neuronal activity, either induced or spontaneous, through a slew of genetic and experimental approaches to disrupt olfactory neuron activation. The authors went on to provide evidence that the type III adenylyl cyclase (ACIII), a key olfactory transduction component in the olfactory cilia, was permissive for the establishment or maintenance of the ciliary length pattern, as ACIII gene knockout resulted in shortened yet uniform ciliary length across the dorsal epithelium. Whether or how ACIII may play an instructive role remains to be determined. Future studies are needed in order to understand the mechanisms controlling the ciliary length and the length pattern in the olfactory periphery and elsewhere. Sensory systems have adopted a variety of mechanisms to achieve a common goal: to enhance detection and discrimination. The findings by Challis et al. [1] provide evidence of a novel organization model of peripheral sensory neurons within the olfactory system, where the most sensitive sensors are localized to the most strongly stimulated areas to ensure the best detection of certain odorants. The discovery adds an
9. Grosmaitre, X., Vassalli, A., Mombaerts, P., Shepherd, G.M., and Ma, M. (2006). Odorant responses of olfactory sensory neurons expressing the odorant receptor MOR23: a patch clamp analysis in gene-targeted mice. Proc. Natl. Acad. Sci. USA 103, 1970–1975.
important, previously overlooked, aspect to our understanding of olfactory coding. REFERENCES 1. Challis, R.C., Tian, H., Wang, J., He, J., Jiang, J., Chen, X., Yin, W., Connelly, T., Ma, L., Yu, C.R., et al. (2015). An olfactory cilia pattern in the mammalian nose ensures high sensitivity to odors. Curr. Biol. 25, 2503–2512. 2. Buck, L., and Axel, R. (1991). A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65, 175–187. 3. Magklara, A., and Lomvardas, S. (2013). Stochastic gene expression in mammals: lessons from olfaction. Trends Cell Biol. 23, 449–456.
10. Morrison, E.E., and Costanzo, R.M. (1990). Morphology of the human olfactory epithelium. J. Comp. Neurol. 297, 1–13. 11. Menco, B.P., and Morrison, E.E. (2003). Morphology of the mammalian olfactory epithelium: form, fine structure, function, and pathology. In Handbook on Olfaction and Gustation, R.L. Doty, ed. (New York: Informa Health Care), pp. 17–49. 12. Schoenfeld, T.A., and Cleland, T.A. (2006). Anatomical contributions to odorant sampling and representation in rodents: zoning in on sniffing behavior. Chem. Senses 31, 131–144.
4. Ressler, K.J., Sullivan, S.L., and Buck, L.B. (1993). A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73, 597–609.
13. Bozza, T., Feinstein, P., Zheng, C., and Mombaerts, P. (2002). Odorant receptor expression defines functional units in the mouse olfactory system. J. Neurosci. 22, 3033–3043.
5. Vassar, R., Ngai, J., and Axel, R. (1993). Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell 74, 309–318.
14. Zhang, X., and Firestein, S. (2002). The olfactory receptor gene superfamily of the mouse. Nat. Neurosci. 5, 124–133.
6. Horowitz, L.F., Saraiva, L.R., Kuang, D., Yoon, K.H., and Buck, L.B. (2014). Olfactory receptor patterning in a higher primate. J. Neurosci. 34, 12241–12252.
15. Zhao, K., Dalton, P., Yang, G.C., and Scherer, P.W. (2006). Numerical modeling of turbulent and laminar airflow and odorant transport during sniffing in the human and rat nose. Chem. Senses 31, 107–118.
7. Scott, J.W., Sherrill, L., Jiang, J., and Zhao, K. (2014). Tuning to odor solubility and sorption pattern in olfactory epithelial responses. J. Neurosci. 34, 2025–2036.
16. van Reeuwijk, J., Arts, H.H., and Roepman, R. (2011). Scrutinizing ciliopathies by unraveling ciliary interaction networks. Hum. Mol. Genet. 20, R149–R157.
8. Yang, G.C., Scherer, P.W., Zhao, K., and Mozell, M.M. (2007). Numerical modeling of odorant uptake in the rat nasal cavity. Chem. Senses 32, 273–284.
17. McIntyre, J.C., Williams, C.L., and Martens, J.R. (2013). Smelling the roses and seeing the light: gene therapy for ciliopathies. Trends Biotechnol. 31, 355–363.
Animal Navigation: Birds Have Magnetic Maps James L. Gould Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544, USA Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2015.08.041
New ‘virtual displacement’ experiments demonstrate that migrating reed warblers know the magnetic coordinates of their destination, and can set a novel course to their goal with only magnetic-field parameters as a guide. The eerie ability of homing pigeons to return more or less directly to their loft after being taken hundreds of kilometers away to an unfamiliar site, often in sensory isolation, has captured the imagination of generations of scientists. This ability, the
behavioral mystery of mysteries — often inaccurately referred to as the ‘animal GPS’ — was distilled into two major competing hypotheses just over 30 years ago [1,2]. Wallraff [1], attempting to account for a series of anomalies in the
homing of birds reared in restrictive ‘palisade’ lofts, proposed that animals learn a radial map based on incoming wind-borne odors, extrapolating the scents out into the wider world. Attempting to account for a series of
R836 Current Biology 25, R827–R844, October 5, 2015 ª2015 Elsevier Ltd All rights reserved
Current Biology
Dispatches anomalies in the homing of pigeons reared in more conventional and naturalistic lofts, I [2] proposed that the birds learn the gradients of total and vertical magnetic-field intensity during play flights near home and extrapolate them into the world beyond. (More recently, a theory based on infrasonic beacons has been advanced [3].) Whichever hypothesis is correct, the resulting ability is not restricted to a single species of bird: adult white-crowned sparrows captured in the Pacific northwest of the US on their southward migration from Canada to Mexico and transported east 4000 km will, upon release, take up a novel WSW heading toward their wintering grounds [4]. An enormous and disparate series of subsequent tests on pigeons has shown that nearly any result is possible depending on rearing and testing conditions [5]. It may be that pigeons are too complex (or subtle, or finicky) in their behavior for our own good. In fact, three sets of tests [6–8] with non-avian subjects that control rigorously for odor show unambiguously that these other species use the earth’s magnetic field as a map. The animals — newts [6], spiny lobsters [7], and sea turtles [8] — are caught, placed in isolation chambers, and subjected to a combination of total and vertical field intensity characteristic of a distant location; they then adopt a heading that (had they actually been moved) would take them back to the magnetic co-ordinates of their point of capture. As they have not actually been taken anywhere, the questions of olfactory orientation and beacons do not arise. As reported in this issue of Current Biology, Kishkinev et al. [9] have extended this ‘virtual displacement’ technique to reed warblers. They took advantage of a previous experiment [10] in which they captured spring migrants en route northeast from Europe to the Russian Arctic, displaced them 1000 km east, and showed that the birds attempted to escape toward their original goal using a novel northwest heading. This does not tell us how the map works; farfetched as it seems, olfactory information might conceivably have been involved. The new experiment [9] finesses the question of sensory alternatives by testing the
animals at the capture site itself, providing the vertical and total magnetic field co-ordinates of the same 1000-km-east location. The authors used an elaborate double-wrapped Merritt four-coil system to create unprecedented field homogeneity, which may account for their impressively clean results: a clear preference for the same novel northwesterly heading toward the summer range along the Russian–Finnish border previously seen when the warblers were physically displaced. Now that we know that the bird map is organized along the same lines as the maps of amphibians, reptiles, and decapods, a new set of questions arises. Homing pigeons seem clearly different from at least white-crowned sparrows in their strategy of calibration — or at least in its timing. For non-migrants like pigeons to be able to home using the earth’s field, they must measure the strength and gradient (both direction and slope) of both the vertical and total field near the loft [2,5]. Given that 12-week-old homers can orient based solely on magnetic information at the release site, the calibration must occur during play flights near the loft between six and 12 weeks of age. With this information, they can then extrapolate up to a few hundred kilometers. The calibration strategy for migrants may be different. Most first-year birds migrate to their winter range at night and along an innate vector (or a sequential set of vectors), stopping based at least in part on an innately recognized latitude value [5]. The white-crowned sparrows captured in the fall consist of a mix of first-year animals and adults. (The reed warblers have all made the journey south at least once before.) After the 4000 km eastward displacement described earlier [4], young birds flew the same southward vector they adopted at the start of their journey from the breeding grounds in Canada, while the adults took up the dramatically novel WSW heading toward the winter habitat. This implies that the first-year sparrows calibrate themselves en route south, or once they reach their goal, learning enough to extrapolate (at least roughly) to the American east coast. And to account for the more modest distances the warblers can deal with, the fledgling birds must do the same for the breeding grounds.
Three general questions need attention now. The first is the range of the migrants’ ability to infer their location after apparent displacement. If the map sense is a true animal GPS, the range is global. But a study of magnetic contours on planet Earth suggests that beyond a few hundred kilometers the various nonlinearities in the pattern would render it increasingly unreliable. The virtual-displacement technique could be used to establish the range and declining accuracy of this remarkable map. Another crucial question is the spatial accuracy of the system. At present we know only that pigeons can get to within a (very) few kilometers of the loft without visual input [11]. Migrants heading south might not need to be this accurate, but those heading back to a specific home in the spring might well want to be far more precise. Reliable measurements based on ever-smaller virtual displacements would also tell us something important about the sensory system (which must depend on accurately measuring both magnetic field strength and the direction of gravity). Finally, the apparent time course and strategy of calibration in map-equipped animals are at present mostly matters of inference and conjecture. Longitudinal (in the temporal rather than navigational sense) or sequential studies need to be done, again using virtual displacement. The orchestration of the leaning programs involved in the calibration of complex innate behavior is one of ethology’s most fascinating problems [12]. REFERENCES 1. Wallraff, H.G. (1981). The olfactory component of pigeon navigation. J. Comp. Physiol. 143, 411–422. 2. Gould, J.L. (1982). The map sense of pigeons. Nature 296, 205–211. 3. Hagstrum, J.T. (2013). Atmospheric propagation modeling indicates homing pigeons use loft-specific infrasonic ‘‘map’’ cues. J. Exp. Biol. 216, 687–699. 4. Thorup, K., Bisson, I.A., Bowlin, M.S., Holland, R.A., Wingfield, J.C., Ramenofsky, R., and Wikelski, M. (2007). Evidence for a navigational map stretching across the continental U.S. in a migratory songbird. Proc. Natl. Acad. Sci. USA 104, 18115–181159. 5. Gould, J.L., and Gould, C.G. (2012). Nature’s Compass: The Mystery of Animal Navigation (Princeton: Princeton University Press).
Current Biology 25, R827–R844, October 5, 2015 ª2015 Elsevier Ltd All rights reserved R837
Current Biology
Dispatches 6. Phillips, J.B., Freake, M.J., Fischer, J.H., and Borland, S.C. (2002). Behavioral titration of a magnetic map coordinate. J. Comp. Physiol. A 188, 157–160. 7. Boles, L.C., and Lohmann, K.J. (2003). True navigation and magnetic maps in spiny lobsters. Nature 421, 60–63. 8. Lohmann, K.J., Lohmann, C.M.F., Ehrhart, L.M., Bagley, D.A., and Swing, K. (2004).
Geomagnetic map used in sea turtle navigation. Nature 428, 909. 9. Kishkinev, D., Chernetsov, N., Pakhomov, A., Heyers, D., and Mouritsen, H. (2015). Eurasian reed warblers compensate for virtual magnetic displacement. Curr. Biol. 25, R822–R824. 10. Chernetsov, N., Kishkinev, D., and Mouritsen, H. (2008). A long-distance avian migrant compensates for longitudinal displacement
during spring migration. Curr. Biol. 18, 188–190. 11. Schmidt-Koenig, K., and Walcott, C. (1978). Tracks of pigeon homing with frosted lenses. Anim. Behav. 26, 480–486. 12. Gould, J.L., and Marler, P. (1984). Ethology and the natural history of learning. In The Biology of Learning, P. Marler, and H. Terrace, eds. (Berlin: Springer-Verlag), pp. 47–74.
Stomatal Patterning: SERKs Put the Mouths in Their Right Place Alice Y. Cheung1,2,3,* and Hen-Ming Wu1,2 1Department
of Biochemistry and Molecular Biology, University of Massachusetts, Amherst, MA 01003, USA and Cell Biology Graduate Program, University of Massachusetts, Amherst, MA 01003, USA 3Plant Biology Graduate Program, University of Massachusetts, Amherst, MA 01003, USA *Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2015.08.049 2Molecular
Plants have stomata, mouth-like pores on their surface, to adjust to environmental changes such as temperature and humidity to ensure optimum physiology and metabolism. A new study adds a key player, SERK, to the signal-sensing apparatus to inform where stomata are to be formed on the leaf. Stomata are apertures on the aerial surfaces of plants that control the uptake and release of water vapor and gaseous exchange in response to environmental conditions and endogenous signals. These apertures are formed by two guard cells (Figure 1A), which also control the opening and closing of the pore. Possibly as a strategy to adapt the physiology of a sessile lifestyle to advantageously co-exist with an ever-changing environment, plants have evolved an elaborate mechanism to regulate how stomata are positioned on the leaf surface, avoiding over-crowdedness and following what is referred to as the ‘one-cell spacing’ rule, which prohibits the differentiation of two adjacent cells into stomata (Figure 1) [1,2]. A cell surface-located signal receptor complex controls stomatal patterning. It comprises one of three related receptor-like kinases (RLKs), ERECTA (ER) and ERECTA-LIKE 1 and 2 (ERL1, ERL2), and a signal modulator, TOO MANY MOUTHS (TMM). Several related peptide molecules, EPIDERMAL PATTERNING FACTORS 1 and 2 (EPF1 and 2) and EPF-like STOMAGEN, differentially bind to the two
components of the receptor–modulator complex to regulate its signaling capacity. A cytoplasmic MAP kinase (MAPK) cascade, composed of the MAPK kinase kinase YODA, the MAPK kinases MKK4/ MKK5 and the MAPKs MPK3/MPK6, control the nuclear activities important for stomatal patterning. The functions of several transcription factors with names befitting their key roles in defining stomatal patterning — SPEECHLESS, SCREAMs, MUTE and FAMA (goddess of rumor) — have also been thoroughly characterized. Recently in Current Biology, Meng et al. [3], in an extensive series of genetic and biochemical experiments, demonstrate that SERKs — SOMATIC EMBRYOGENESIS RECEPTOR KINASES — are part of the signaling ensemble that regulates stomatal development in Arabidopsis (Figure 1B). This discovery not only further elaborates the regulatory network that underlies one of nature’s most intricate designs, but also underscores the functional versatility of SERKs, which are known to play central roles in diverse processes, including steroid hormone brassinolide-regulated development,
male gametogenesis and immune response [4]. The first indication for Meng et al. that SERKs might be involved in stomatal patterning came from the observation that overexpressing the effectors AvrPto and AvrPtoB, from the bacterial pathogen Pseudomonas syringae, induced excessive clustering of stomata in Arabidopsis, violating the one-cell spacing rule. AvrPto and AvrPtoB are known to target BAK1 (Brassinosteroid insensitive 1 (BRI1)-Associated Kinase, also named SERK3), which interacts with FLAGELLIN SENSING 2 (FLS2) and acts together with FLS2 as a receptor– coreceptor pair to mediate immune response. BAK1 is also a coreceptor in BR signaling, interacting directly with the BRI1–BR receptor ligand complex [4]. The multi-tasking nature of BAK1 therefore further sets the stage for SERKs as also playing a key role in stomatal development. Using a large number of loss-of-function SERK mutants, Meng et al. systematically examined the contribution of each of the four functional SERKs in Arabidopsis — SERK1, SERK2, BAK1 and SERK4 — to stomatal
R838 Current Biology 25, R827–R844, October 5, 2015 ª2015 Elsevier Ltd All rights reserved
Dispatches cilia shapes and sizes. How is the regional ciliary length pattern of the olfactory epithelium established and maintained? Challis et al. [1] have ruled out a role for neuronal activity, either induced or spontaneous, through a slew of genetic and experimental approaches to disrupt olfactory neuron activation. The authors went on to provide evidence that the type III adenylyl cyclase (ACIII), a key olfactory transduction component in the olfactory cilia, was permissive for the establishment or maintenance of the ciliary length pattern, as ACIII gene knockout resulted in shortened yet uniform ciliary length across the dorsal epithelium. Whether or how ACIII may play an instructive role remains to be determined. Future studies are needed in order to understand the mechanisms controlling the ciliary length and the length pattern in the olfactory periphery and elsewhere. Sensory systems have adopted a variety of mechanisms to achieve a common goal: to enhance detection and discrimination. The findings by Challis et al. [1] provide evidence of a novel organization model of peripheral sensory neurons within the olfactory system, where the most sensitive sensors are localized to the most strongly stimulated areas to ensure the best detection of certain odorants. The discovery adds an
9. Grosmaitre, X., Vassalli, A., Mombaerts, P., Shepherd, G.M., and Ma, M. (2006). Odorant responses of olfactory sensory neurons expressing the odorant receptor MOR23: a patch clamp analysis in gene-targeted mice. Proc. Natl. Acad. Sci. USA 103, 1970–1975.
important, previously overlooked, aspect to our understanding of olfactory coding. REFERENCES 1. Challis, R.C., Tian, H., Wang, J., He, J., Jiang, J., Chen, X., Yin, W., Connelly, T., Ma, L., Yu, C.R., et al. (2015). An olfactory cilia pattern in the mammalian nose ensures high sensitivity to odors. Curr. Biol. 25, 2503–2512. 2. Buck, L., and Axel, R. (1991). A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65, 175–187. 3. Magklara, A., and Lomvardas, S. (2013). Stochastic gene expression in mammals: lessons from olfaction. Trends Cell Biol. 23, 449–456.
10. Morrison, E.E., and Costanzo, R.M. (1990). Morphology of the human olfactory epithelium. J. Comp. Neurol. 297, 1–13. 11. Menco, B.P., and Morrison, E.E. (2003). Morphology of the mammalian olfactory epithelium: form, fine structure, function, and pathology. In Handbook on Olfaction and Gustation, R.L. Doty, ed. (New York: Informa Health Care), pp. 17–49. 12. Schoenfeld, T.A., and Cleland, T.A. (2006). Anatomical contributions to odorant sampling and representation in rodents: zoning in on sniffing behavior. Chem. Senses 31, 131–144.
4. Ressler, K.J., Sullivan, S.L., and Buck, L.B. (1993). A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73, 597–609.
13. Bozza, T., Feinstein, P., Zheng, C., and Mombaerts, P. (2002). Odorant receptor expression defines functional units in the mouse olfactory system. J. Neurosci. 22, 3033–3043.
5. Vassar, R., Ngai, J., and Axel, R. (1993). Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell 74, 309–318.
14. Zhang, X., and Firestein, S. (2002). The olfactory receptor gene superfamily of the mouse. Nat. Neurosci. 5, 124–133.
6. Horowitz, L.F., Saraiva, L.R., Kuang, D., Yoon, K.H., and Buck, L.B. (2014). Olfactory receptor patterning in a higher primate. J. Neurosci. 34, 12241–12252.
15. Zhao, K., Dalton, P., Yang, G.C., and Scherer, P.W. (2006). Numerical modeling of turbulent and laminar airflow and odorant transport during sniffing in the human and rat nose. Chem. Senses 31, 107–118.
7. Scott, J.W., Sherrill, L., Jiang, J., and Zhao, K. (2014). Tuning to odor solubility and sorption pattern in olfactory epithelial responses. J. Neurosci. 34, 2025–2036.
16. van Reeuwijk, J., Arts, H.H., and Roepman, R. (2011). Scrutinizing ciliopathies by unraveling ciliary interaction networks. Hum. Mol. Genet. 20, R149–R157.
8. Yang, G.C., Scherer, P.W., Zhao, K., and Mozell, M.M. (2007). Numerical modeling of odorant uptake in the rat nasal cavity. Chem. Senses 32, 273–284.
17. McIntyre, J.C., Williams, C.L., and Martens, J.R. (2013). Smelling the roses and seeing the light: gene therapy for ciliopathies. Trends Biotechnol. 31, 355–363.
Animal Navigation: Birds Have Magnetic Maps James L. Gould Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544, USA Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2015.08.041
New ‘virtual displacement’ experiments demonstrate that migrating reed warblers know the magnetic coordinates of their destination, and can set a novel course to their goal with only magnetic-field parameters as a guide. The eerie ability of homing pigeons to return more or less directly to their loft after being taken hundreds of kilometers away to an unfamiliar site, often in sensory isolation, has captured the imagination of generations of scientists. This ability, the
behavioral mystery of mysteries — often inaccurately referred to as the ‘animal GPS’ — was distilled into two major competing hypotheses just over 30 years ago [1,2]. Wallraff [1], attempting to account for a series of anomalies in the
homing of birds reared in restrictive ‘palisade’ lofts, proposed that animals learn a radial map based on incoming wind-borne odors, extrapolating the scents out into the wider world. Attempting to account for a series of
R836 Current Biology 25, R827–R844, October 5, 2015 ª2015 Elsevier Ltd All rights reserved
Current Biology
Dispatches anomalies in the homing of pigeons reared in more conventional and naturalistic lofts, I [2] proposed that the birds learn the gradients of total and vertical magnetic-field intensity during play flights near home and extrapolate them into the world beyond. (More recently, a theory based on infrasonic beacons has been advanced [3].) Whichever hypothesis is correct, the resulting ability is not restricted to a single species of bird: adult white-crowned sparrows captured in the Pacific northwest of the US on their southward migration from Canada to Mexico and transported east 4000 km will, upon release, take up a novel WSW heading toward their wintering grounds [4]. An enormous and disparate series of subsequent tests on pigeons has shown that nearly any result is possible depending on rearing and testing conditions [5]. It may be that pigeons are too complex (or subtle, or finicky) in their behavior for our own good. In fact, three sets of tests [6–8] with non-avian subjects that control rigorously for odor show unambiguously that these other species use the earth’s magnetic field as a map. The animals — newts [6], spiny lobsters [7], and sea turtles [8] — are caught, placed in isolation chambers, and subjected to a combination of total and vertical field intensity characteristic of a distant location; they then adopt a heading that (had they actually been moved) would take them back to the magnetic co-ordinates of their point of capture. As they have not actually been taken anywhere, the questions of olfactory orientation and beacons do not arise. As reported in this issue of Current Biology, Kishkinev et al. [9] have extended this ‘virtual displacement’ technique to reed warblers. They took advantage of a previous experiment [10] in which they captured spring migrants en route northeast from Europe to the Russian Arctic, displaced them 1000 km east, and showed that the birds attempted to escape toward their original goal using a novel northwest heading. This does not tell us how the map works; farfetched as it seems, olfactory information might conceivably have been involved. The new experiment [9] finesses the question of sensory alternatives by testing the
animals at the capture site itself, providing the vertical and total magnetic field co-ordinates of the same 1000-km-east location. The authors used an elaborate double-wrapped Merritt four-coil system to create unprecedented field homogeneity, which may account for their impressively clean results: a clear preference for the same novel northwesterly heading toward the summer range along the Russian–Finnish border previously seen when the warblers were physically displaced. Now that we know that the bird map is organized along the same lines as the maps of amphibians, reptiles, and decapods, a new set of questions arises. Homing pigeons seem clearly different from at least white-crowned sparrows in their strategy of calibration — or at least in its timing. For non-migrants like pigeons to be able to home using the earth’s field, they must measure the strength and gradient (both direction and slope) of both the vertical and total field near the loft [2,5]. Given that 12-week-old homers can orient based solely on magnetic information at the release site, the calibration must occur during play flights near the loft between six and 12 weeks of age. With this information, they can then extrapolate up to a few hundred kilometers. The calibration strategy for migrants may be different. Most first-year birds migrate to their winter range at night and along an innate vector (or a sequential set of vectors), stopping based at least in part on an innately recognized latitude value [5]. The white-crowned sparrows captured in the fall consist of a mix of first-year animals and adults. (The reed warblers have all made the journey south at least once before.) After the 4000 km eastward displacement described earlier [4], young birds flew the same southward vector they adopted at the start of their journey from the breeding grounds in Canada, while the adults took up the dramatically novel WSW heading toward the winter habitat. This implies that the first-year sparrows calibrate themselves en route south, or once they reach their goal, learning enough to extrapolate (at least roughly) to the American east coast. And to account for the more modest distances the warblers can deal with, the fledgling birds must do the same for the breeding grounds.
Three general questions need attention now. The first is the range of the migrants’ ability to infer their location after apparent displacement. If the map sense is a true animal GPS, the range is global. But a study of magnetic contours on planet Earth suggests that beyond a few hundred kilometers the various nonlinearities in the pattern would render it increasingly unreliable. The virtual-displacement technique could be used to establish the range and declining accuracy of this remarkable map. Another crucial question is the spatial accuracy of the system. At present we know only that pigeons can get to within a (very) few kilometers of the loft without visual input [11]. Migrants heading south might not need to be this accurate, but those heading back to a specific home in the spring might well want to be far more precise. Reliable measurements based on ever-smaller virtual displacements would also tell us something important about the sensory system (which must depend on accurately measuring both magnetic field strength and the direction of gravity). Finally, the apparent time course and strategy of calibration in map-equipped animals are at present mostly matters of inference and conjecture. Longitudinal (in the temporal rather than navigational sense) or sequential studies need to be done, again using virtual displacement. The orchestration of the leaning programs involved in the calibration of complex innate behavior is one of ethology’s most fascinating problems [12]. REFERENCES 1. Wallraff, H.G. (1981). The olfactory component of pigeon navigation. J. Comp. Physiol. 143, 411–422. 2. Gould, J.L. (1982). The map sense of pigeons. Nature 296, 205–211. 3. Hagstrum, J.T. (2013). Atmospheric propagation modeling indicates homing pigeons use loft-specific infrasonic ‘‘map’’ cues. J. Exp. Biol. 216, 687–699. 4. Thorup, K., Bisson, I.A., Bowlin, M.S., Holland, R.A., Wingfield, J.C., Ramenofsky, R., and Wikelski, M. (2007). Evidence for a navigational map stretching across the continental U.S. in a migratory songbird. Proc. Natl. Acad. Sci. USA 104, 18115–181159. 5. Gould, J.L., and Gould, C.G. (2012). Nature’s Compass: The Mystery of Animal Navigation (Princeton: Princeton University Press).
Current Biology 25, R827–R844, October 5, 2015 ª2015 Elsevier Ltd All rights reserved R837
Current Biology
Dispatches 6. Phillips, J.B., Freake, M.J., Fischer, J.H., and Borland, S.C. (2002). Behavioral titration of a magnetic map coordinate. J. Comp. Physiol. A 188, 157–160. 7. Boles, L.C., and Lohmann, K.J. (2003). True navigation and magnetic maps in spiny lobsters. Nature 421, 60–63. 8. Lohmann, K.J., Lohmann, C.M.F., Ehrhart, L.M., Bagley, D.A., and Swing, K. (2004).
Geomagnetic map used in sea turtle navigation. Nature 428, 909. 9. Kishkinev, D., Chernetsov, N., Pakhomov, A., Heyers, D., and Mouritsen, H. (2015). Eurasian reed warblers compensate for virtual magnetic displacement. Curr. Biol. 25, R822–R824. 10. Chernetsov, N., Kishkinev, D., and Mouritsen, H. (2008). A long-distance avian migrant compensates for longitudinal displacement
during spring migration. Curr. Biol. 18, 188–190. 11. Schmidt-Koenig, K., and Walcott, C. (1978). Tracks of pigeon homing with frosted lenses. Anim. Behav. 26, 480–486. 12. Gould, J.L., and Marler, P. (1984). Ethology and the natural history of learning. In The Biology of Learning, P. Marler, and H. Terrace, eds. (Berlin: Springer-Verlag), pp. 47–74.
Stomatal Patterning: SERKs Put the Mouths in Their Right Place Alice Y. Cheung1,2,3,* and Hen-Ming Wu1,2 1Department
of Biochemistry and Molecular Biology, University of Massachusetts, Amherst, MA 01003, USA and Cell Biology Graduate Program, University of Massachusetts, Amherst, MA 01003, USA 3Plant Biology Graduate Program, University of Massachusetts, Amherst, MA 01003, USA *Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2015.08.049 2Molecular
Plants have stomata, mouth-like pores on their surface, to adjust to environmental changes such as temperature and humidity to ensure optimum physiology and metabolism. A new study adds a key player, SERK, to the signal-sensing apparatus to inform where stomata are to be formed on the leaf. Stomata are apertures on the aerial surfaces of plants that control the uptake and release of water vapor and gaseous exchange in response to environmental conditions and endogenous signals. These apertures are formed by two guard cells (Figure 1A), which also control the opening and closing of the pore. Possibly as a strategy to adapt the physiology of a sessile lifestyle to advantageously co-exist with an ever-changing environment, plants have evolved an elaborate mechanism to regulate how stomata are positioned on the leaf surface, avoiding over-crowdedness and following what is referred to as the ‘one-cell spacing’ rule, which prohibits the differentiation of two adjacent cells into stomata (Figure 1) [1,2]. A cell surface-located signal receptor complex controls stomatal patterning. It comprises one of three related receptor-like kinases (RLKs), ERECTA (ER) and ERECTA-LIKE 1 and 2 (ERL1, ERL2), and a signal modulator, TOO MANY MOUTHS (TMM). Several related peptide molecules, EPIDERMAL PATTERNING FACTORS 1 and 2 (EPF1 and 2) and EPF-like STOMAGEN, differentially bind to the two
components of the receptor–modulator complex to regulate its signaling capacity. A cytoplasmic MAP kinase (MAPK) cascade, composed of the MAPK kinase kinase YODA, the MAPK kinases MKK4/ MKK5 and the MAPKs MPK3/MPK6, control the nuclear activities important for stomatal patterning. The functions of several transcription factors with names befitting their key roles in defining stomatal patterning — SPEECHLESS, SCREAMs, MUTE and FAMA (goddess of rumor) — have also been thoroughly characterized. Recently in Current Biology, Meng et al. [3], in an extensive series of genetic and biochemical experiments, demonstrate that SERKs — SOMATIC EMBRYOGENESIS RECEPTOR KINASES — are part of the signaling ensemble that regulates stomatal development in Arabidopsis (Figure 1B). This discovery not only further elaborates the regulatory network that underlies one of nature’s most intricate designs, but also underscores the functional versatility of SERKs, which are known to play central roles in diverse processes, including steroid hormone brassinolide-regulated development,
male gametogenesis and immune response [4]. The first indication for Meng et al. that SERKs might be involved in stomatal patterning came from the observation that overexpressing the effectors AvrPto and AvrPtoB, from the bacterial pathogen Pseudomonas syringae, induced excessive clustering of stomata in Arabidopsis, violating the one-cell spacing rule. AvrPto and AvrPtoB are known to target BAK1 (Brassinosteroid insensitive 1 (BRI1)-Associated Kinase, also named SERK3), which interacts with FLAGELLIN SENSING 2 (FLS2) and acts together with FLS2 as a receptor– coreceptor pair to mediate immune response. BAK1 is also a coreceptor in BR signaling, interacting directly with the BRI1–BR receptor ligand complex [4]. The multi-tasking nature of BAK1 therefore further sets the stage for SERKs as also playing a key role in stomatal development. Using a large number of loss-of-function SERK mutants, Meng et al. systematically examined the contribution of each of the four functional SERKs in Arabidopsis — SERK1, SERK2, BAK1 and SERK4 — to stomatal
R838 Current Biology 25, R827–R844, October 5, 2015 ª2015 Elsevier Ltd All rights reserved