- Email: [email protected]
Orienting Movements: Brainstem Neurons at the Wheel
ll 17. Akc¸akaya, H.R., Keith, D.A., Burgman, M., Butchart, S.H.M., Hoffmann, M., Regan, H.M., Harrison, I., and Boakes, E. (2017). Inferring extinctions III: A cost-benefit framework for listing extinct species. Biol. Conserv. 214, 336–342. 18. Thurstan, R.H., McClenachan, L., Crowder, L.B., Drew, J.A., Kittinger, J.N., Levin, P.S.,
Dispatches Roberts, C.M., and Pandolfi, J.M. (2015). Filling historical data gaps to foster solutions in marine conservation. Ocean Coast. Manag. 115, 31–40. 19. Cinner, J.E., and McClanahan, T.R. (2006). Socioeconomic factors that lead to overfishing in small-scale coral reef fisheries
of Papua New Guinea. Environ. Conserv. 33, 73–80. 20. Jennings, S., and Polunin, N.V.C. (1995). Effects of fishing on the biomass and structure of target reef fish communities. J. Appl. Ecol. 33, 400–412.
Orienting Movements: Brainstem Neurons at the Wheel Zane Mitrevica and Andrew J. Murray* Sainsbury Wellcome Centre for Neural Circuits and Behaviour, University College London, London W1T 4JG, UK *Correspondence: [email protected] https://doi.org/10.1016/j.cub.2020.09.060
The nervous system must constantly adjust its motor output in response to changes in the environment. A new study of the control of orienting movements in mice has identified discrete groups of neurons in the brainstem that connect a sensory integrative area with distinct features of motor behaviour. Whether you are a mouse chasing a hopping cricket, or a human negotiating a crowded footpath, your nervous system must quickly use the percept of the environment to generate and execute a motor plan that guides you safely to your goal. Though we are generally able to perform these behaviours seamlessly, and without conscious thought, they are made up of multiple motor elements that depend on circuits throughout the nervous system. Consider for example a mouse chasing its prey. A sudden change in heading direction of the cricket forces the mouse to do the same. First, the change in direction must be perceived by the visual system, which must also be aware of any potential obstacles in the vicinity. Then, to maintain the cricket in the visual field, the eyes and head must be reoriented, requiring coordination of the visual system with the musculature controlling the eyes and neck. Next, before turning, the mouse will slow its own motor speed so as to not take a corner too quickly and topple over. Finally, all four limbs must be coordinated along with curvature of the body to rotate around to the new heading. Many components of the motor circuitry underlying these behaviours — start, stop, turn, accelerate — have
been described, but how is the entire movement coordinated, and how does the motor circuitry implementing the movement link to perceptual circuits that instruct the change in direction? As they report in this issue of Current Biology, Usseglio et al. [1] have addressed these questions with results that implicate brainstem neurons in connecting sensory input with motor behaviour. Movement, and in particular our ability to generate coordinated and goaldirected locomotion, is central to animal survival. We have known for over 100 years that the spinal cord is capable of generating the rhythmic movements at the core of locomotion. Thomas Graham Brown [2,3] was among the first to postulate that groups of interneurons in the isolated spinal cord could generate the locomotor rhythm even in the absence of sensory feedback or descending control from the brain. Since these early studies, many researchers have confirmed Graham Brown’s observations and picked apart the identities of the various neural components. The spinal cord indeed contains an impressive repertoire of circuits, with numerous classes of spinal interneurons having now been identified and categorised according to transcription factor
R1418 Current Biology 30, R1413–R1441, December 7, 2020 ª 2020 Elsevier Inc.
expression, electrophysiological properties and ultimately function [4–7]. Much like a car engine is not useful in isolation, however, the spinal cord cannot coordinate movement alone. This requires multiple descending pathways from the brain (Figure 1). Instructing the spinal circuits to initiate or alter the speed of locomotion involves a discrete region in the mammalian brain known as the mesencephalic locomotor region, or MLR. Electrical stimulation of this highly conserved area initiates movement, the speed of which is directly related to stimulus intensity [8]. A recent series of elegant viral and genetic studies identified subtypes of neurons in the MLR that control either fast or slow locomotion [9,10], as well as some of their medullary actuators in the lateral paragigantocellular nucleus [11]. Similarly, termination of locomotion has been linked to a discrete population of V2a neurons (named for their developmental origin) in the reticular formation of the brainstem [12]. Following the analogy of driving a car these can be considered as the ignition, accelerator and brake. But what about the steering wheel? How do we turn a corner? The superior colliculus has an established role in orienting behaviour, hosting a map of combinatorial head displacement vectors [13,14]. Yet, the downstream circuits
ll
Dispatches implementing turns of the head and the body are only beginning to be described [11,15]. Usseglio et al. [1] set out to understand these circuits. In search of brainstem neurons responsible for orienting commands, Usseglio et al. [1] also probed the function of V2a-derived neurons — those located in rostral medullary reticular formation, predominantly the gigantocellular nucleus (Gi). This region receives input from the superior colliculus and sends a direct projection to the spinal cord, providing a potential pathway from sensory perception and integration to motor output. Using a modified rabies virus, the authors traced the monosynaptic inputs to V2a Gi neurons and indeed found a prominent direct pathway between these neurons and the superior colliculus. Further inputs were observed in the deep cerebellar nuclei, some midbrain nuclei, as well as the local circuitry. This positions the V2a Gi neurons in the appropriate anatomical position for relaying asymmetric motor commands to the spinal cord. Having established that V2a Gi neurons possess the anatomical connections required for an involvement in orientation behaviour, Usseglio et al. [1] probed their function. Given a previous report of these neurons halting locomotion when stimulated bilaterally [12], unilateral activation of these neurons could reasonably be expected to evoke asymmetric braking and turn the body to the more rapidly decelerating side. In fact, a recent study [15] conducted independently of Usseglio et al. [1] proposed this as the mechanism controlling locomotor trajectory. Recapitulating the findings of that work, unilateral stimulation of V2a Gi neurons led mice to decelerate and change their heading direction towards the stimulated side. Similarly, frequent turning to the opposite side during locomotion was observed upon unilateral silencing of these neurons. Intriguingly, however, stimulation experiments in stationary animals painted a more complicated picture of V2a function than a simple asymmetric braking. For instance, reminiscent of earlier findings with a larger population of glutamatergic Gi neurons [11], unrestrained mice responded to unilateral V2a stimulation by horizontally reorienting their head and body even when at rest. With those movements prevented through head-fixing, the same stimulation protocol evoked deflection of the snout
SUPERIOR COLLICULUS Headlights Sensory integration & orienting vectors
MESENCEPHALIC LOCOMOTOR REGION Ignition & gas pedal Locomotion intiation & speed setting
LATERAL PARAGIGANTOCELLULAR NUCLEUS Spark plug & throttle valve Locomotion intiation relay & speed control
GIGANTOCELLULAR NUCLEUS Wheel & brake pedal Locomotion steering & termination
SPINAL CORD Engine Rhythm generation Coordinated control of flexor & extensor muscles within and across body parts F
E
Flexor and extensor half-centres Current Biology
Figure 1. Brainstem motor centres reimagined as an automobile. As shown by Usseglio et al. [1], the gigantocellular nucleus is analogous to the brakes and the steering wheel of locomotion, guided by superior colliculus. In parallel, the mesencephalic locomotor region (MLR) initiates, and sets the speed of, locomotion, functioning as both the ignition system and the gas pedal. Downstream of these, the spark plug and the throttle valve control the engine, much like the lateral paragigantocellular nucleus communicates information from the MLR to the spinal cord.
along the horizontal axis. Notably, these motor elements — snout deflection, head rotation, body reorientation — were evoked with distinct latencies, and occurred in the same temporal sequence as during self-generated changes in locomotor trajectory. As these movements were not necessarily accompanied by deceleration, this implicates the brainstem V2a neurons in orienting movements beyond those associated with left–right asymmetric activity of the limbs, and tentatively decouple their roles in steering and braking. How could such diverse motor outputs be generated by a single population of brainstem neurons? Usseglio et al. [1] reasoned that the population would require access to multiple motor circuits, and so mapped the axons of these neurons through selective expression of a fluorescent protein. They found dense innervation of regions involved in movements of the snout, whiskers, neck and hindlimb. But do all V2a Gi neurons have the same projection pattern and, presumably, function? The authors addressed this by using a series of retrograde tracing approaches targeted to the cervical and lumbar spinal cord
segments, controlling movements of the neck and hindlimb, respectively. This experiment uncovered subsets of V2a neurons that project to either cervical or lumbar levels, but very rarely both, showing that there are multiple projection-defined V2a Gi cell types. Stimulation of these individual neuron types revealed a remarkable division of orienting and locomotor behaviours. Unilateral stimulation of only the lumbarprojecting V2a neurons halted locomotion without changing movement trajectory, much like upon bilateral V2a stimulation in the brainstem [12]. Conversely, selective activation of the cervical-projecting V2a neurons resulted in head rotation and body reorientation, with no significant effect on locomotor speed. Considering the distinct behavioural specialisations of these V2a subpopulations and their additive effects during collective activation, it is tempting to imagine how dynamic mixing and matching of these separate pathways’ activities could result in a highly versatile controller employable in wide-ranging contexts. Like a Swiss army knife of motor coordination, this system could aid responses as diverse as whole-body freezing when under a threat,
Current Biology 30, R1413–R1441, December 7, 2020 R1419
ll a head rotation towards a familiar sound, and, indeed, a well-calibrated turn around the corner by a mouse chasing its meal. There are still many aspects of orienting movements that we do not understand. How, for example, does the nervous system learn to recruit these motor modules in a behaviourally relevant fashion? Or, what is the circuit logic linking V2a Gi neurons with the various spinal inter- and motor neurons that produce the behaviour? The study by Usseglio et al. [1] takes an important step to answering such questions around this important behaviour. REFERENCES , A., He rent, C., 1. Usseglio, G., Gatier, E., Heuze and Bouvier, J. (2020). Control of orienting movements and locomotion by projectiondefined subsets of brainstem V2a neurons. Curr. Biol. 30, 4665–4681. 2. Graham-Brown, T. (1911). The intrinsic factors in the act of progression in the mammal. Proc. R. Soc. Lond. B 84, 309–319.
Dispatches 3. Graham-Brown, T. (1914). On the nature of the fundamental activity of the nervous centres; together with an analysis of the conditioning of rhythmic activity in progression, and a theory of the evolution of function in the nervous system. J. Physiol. 48, 18–46.
10. Josset, N., Roussel, M., Lemieux, M., Lafrance-Zougba, D., Rastqar, A., and Bretzner, F. (2018). Distinct contributions of mesencephalic locomotor region nuclei to locomotor control in the freely behaving mouse. Curr. Biol. 28, 884–901.
4. Goulding, M. (2009). Circuits controlling vertebrate locomotion: moving in a new direction. Nat. Rev. Neurosci. 10, 507–518.
11. Capelli, P., Pivetta, C., Soledad Esposito, M., and Arber, S. (2017). Locomotor speed control circuits in the caudal brainstem. Nature 551, 373–377.
5. Jessell, T.M. (2000). Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1, 20–29. 6. Kiehn, O. (2016). Decoding the organization of spinal circuits that control locomotion. Nat. Rev. Neurosci. 17, 224–238. 7. Arber, S. (2011). Motor circuits in action: specification, connectivity, and function. Neuron 74, 975–989.
12. Bouvier, J., Caggiano, V., Leiras, R., Caldeira, V., Bellardita, C., Balueva, K., Fuchs, A., and Kiehn, O. (2015). Descending command neurons in the brainstem that halt locomotion. Cell 163, 1191–1203. 13. Gandhi, N.J., and Katnani, H.A. (2011). Motor functions of the superior colliculus. Annu. Rev. Neurosci. 34, 205–231.
8. Shik, M.L., and Orlovsky, G.N. (1976). Neurophysiology of locomotor automatism. Physiol. Rev. 56, 465–501.
14. Massulo, L., Mariotti, L., Alexandre, N., FreirePritchett, P., Boulanger, J., and Tripodi, M. (2019). Genetically defined functional modules for spatial orienting in the mouse superior colliculus. Curr. Biol. 29, 2892–2904.
9. Caggiano, V., Leiras, R., Goni-Erro, H., Masini, D., Bellardita, C., Bouvier, J., Caldeira, V., Fisone, G., and Kiehn, O. (2018). Midbrain circuits that set locomotor speed and gait selection. Nature 553, 455–460.
15. Cregg, J.M., Leiras, R., Montalant, A., Wanker, P., Wickersham, I.R., and Kiehn, O. (2020). Brainstem neurons that command mammalian locomotor asymmetries. Nat. Neurosci. 23, 730–740.
Plant Biology: Gynoecium Development with Style Stefan de Folter
cnico Nacional Unidad de Geno´mica Avanzada (UGA-LANGEBIO), Centro de Investigacio´n y de Estudios Avanzados del Instituto Polite xico (CINVESTAV-IPN), Km 9.6 Libramiento Norte, Carretera Irapuato-Leo´n, C.P. 36824 Irapuato, Me Correspondence: [email protected] https://doi.org/10.1016/j.cub.2020.10.040
The gynoecium is the female reproductive part of the flower and is essential for plant sexual reproduction. A new study shows a novel angiosperm-specific gene family that fine tunes the architecture of the stigma and style in Arabidopsis. Most plant species on earth are angiosperms, which produce flowers. Most flowers produce in their center a gynoecium or pistil, surrounded by the androecium or the stamens. Stamens produce pollen and the pistil produces ovules — these two components are the basis of sexual reproduction in plants. A rich diversity of floral structures, shapes and sizes is present in nature, as well as variations in the process of sexual reproduction. Although, generalizing, pollen grains land on the stigma of the pistil and germinate, and each pollen grain forms a pollen tube to bring its content to the egg cell inside the ovule to fertilize it
(Figure 1) [1–3]. Understanding these simple sounding events, which in reality are enormously complex, is of great interest to many. Many molecular insights come from the model plant Arabidopsis thaliana, which serves as a good genetic system to unravel the gene regulatory networks that guide androecium and gynoecium development [4–7], as well as the networks involved in pollen tube growth and male gametophyte (pollen) interaction with the gynoecium [1–3]. Focusing on the Arabidopsis gynoecium, we can divide the structure into three parts — from top to bottom, the stigma and style form the apical part, the
R1420 Current Biology 30, R1413–R1441, December 7, 2020 ª 2020 Elsevier Inc.
ovary with ovules inside forms the middle part, and the basal part is the gynophore that forms the connection with the mother plant (Figure 1). Various tissue types are present inside the gynoecium; one is called the transmitting tract tissue and produces extracellular matrix, which is a mixture of polysaccharides, glycoproteins, and glycolipids through which pollen tubes will grow when passing through the style and the ovary to reach the ovules [8–10]. Many transcription factors involved in gynoecium development have been identified over the last three decades by many labs [4,6,7,11]. Related to the apical
Dispatches Roberts, C.M., and Pandolfi, J.M. (2015). Filling historical data gaps to foster solutions in marine conservation. Ocean Coast. Manag. 115, 31–40. 19. Cinner, J.E., and McClanahan, T.R. (2006). Socioeconomic factors that lead to overfishing in small-scale coral reef fisheries
of Papua New Guinea. Environ. Conserv. 33, 73–80. 20. Jennings, S., and Polunin, N.V.C. (1995). Effects of fishing on the biomass and structure of target reef fish communities. J. Appl. Ecol. 33, 400–412.
Orienting Movements: Brainstem Neurons at the Wheel Zane Mitrevica and Andrew J. Murray* Sainsbury Wellcome Centre for Neural Circuits and Behaviour, University College London, London W1T 4JG, UK *Correspondence: [email protected] https://doi.org/10.1016/j.cub.2020.09.060
The nervous system must constantly adjust its motor output in response to changes in the environment. A new study of the control of orienting movements in mice has identified discrete groups of neurons in the brainstem that connect a sensory integrative area with distinct features of motor behaviour. Whether you are a mouse chasing a hopping cricket, or a human negotiating a crowded footpath, your nervous system must quickly use the percept of the environment to generate and execute a motor plan that guides you safely to your goal. Though we are generally able to perform these behaviours seamlessly, and without conscious thought, they are made up of multiple motor elements that depend on circuits throughout the nervous system. Consider for example a mouse chasing its prey. A sudden change in heading direction of the cricket forces the mouse to do the same. First, the change in direction must be perceived by the visual system, which must also be aware of any potential obstacles in the vicinity. Then, to maintain the cricket in the visual field, the eyes and head must be reoriented, requiring coordination of the visual system with the musculature controlling the eyes and neck. Next, before turning, the mouse will slow its own motor speed so as to not take a corner too quickly and topple over. Finally, all four limbs must be coordinated along with curvature of the body to rotate around to the new heading. Many components of the motor circuitry underlying these behaviours — start, stop, turn, accelerate — have
been described, but how is the entire movement coordinated, and how does the motor circuitry implementing the movement link to perceptual circuits that instruct the change in direction? As they report in this issue of Current Biology, Usseglio et al. [1] have addressed these questions with results that implicate brainstem neurons in connecting sensory input with motor behaviour. Movement, and in particular our ability to generate coordinated and goaldirected locomotion, is central to animal survival. We have known for over 100 years that the spinal cord is capable of generating the rhythmic movements at the core of locomotion. Thomas Graham Brown [2,3] was among the first to postulate that groups of interneurons in the isolated spinal cord could generate the locomotor rhythm even in the absence of sensory feedback or descending control from the brain. Since these early studies, many researchers have confirmed Graham Brown’s observations and picked apart the identities of the various neural components. The spinal cord indeed contains an impressive repertoire of circuits, with numerous classes of spinal interneurons having now been identified and categorised according to transcription factor
R1418 Current Biology 30, R1413–R1441, December 7, 2020 ª 2020 Elsevier Inc.
expression, electrophysiological properties and ultimately function [4–7]. Much like a car engine is not useful in isolation, however, the spinal cord cannot coordinate movement alone. This requires multiple descending pathways from the brain (Figure 1). Instructing the spinal circuits to initiate or alter the speed of locomotion involves a discrete region in the mammalian brain known as the mesencephalic locomotor region, or MLR. Electrical stimulation of this highly conserved area initiates movement, the speed of which is directly related to stimulus intensity [8]. A recent series of elegant viral and genetic studies identified subtypes of neurons in the MLR that control either fast or slow locomotion [9,10], as well as some of their medullary actuators in the lateral paragigantocellular nucleus [11]. Similarly, termination of locomotion has been linked to a discrete population of V2a neurons (named for their developmental origin) in the reticular formation of the brainstem [12]. Following the analogy of driving a car these can be considered as the ignition, accelerator and brake. But what about the steering wheel? How do we turn a corner? The superior colliculus has an established role in orienting behaviour, hosting a map of combinatorial head displacement vectors [13,14]. Yet, the downstream circuits
ll
Dispatches implementing turns of the head and the body are only beginning to be described [11,15]. Usseglio et al. [1] set out to understand these circuits. In search of brainstem neurons responsible for orienting commands, Usseglio et al. [1] also probed the function of V2a-derived neurons — those located in rostral medullary reticular formation, predominantly the gigantocellular nucleus (Gi). This region receives input from the superior colliculus and sends a direct projection to the spinal cord, providing a potential pathway from sensory perception and integration to motor output. Using a modified rabies virus, the authors traced the monosynaptic inputs to V2a Gi neurons and indeed found a prominent direct pathway between these neurons and the superior colliculus. Further inputs were observed in the deep cerebellar nuclei, some midbrain nuclei, as well as the local circuitry. This positions the V2a Gi neurons in the appropriate anatomical position for relaying asymmetric motor commands to the spinal cord. Having established that V2a Gi neurons possess the anatomical connections required for an involvement in orientation behaviour, Usseglio et al. [1] probed their function. Given a previous report of these neurons halting locomotion when stimulated bilaterally [12], unilateral activation of these neurons could reasonably be expected to evoke asymmetric braking and turn the body to the more rapidly decelerating side. In fact, a recent study [15] conducted independently of Usseglio et al. [1] proposed this as the mechanism controlling locomotor trajectory. Recapitulating the findings of that work, unilateral stimulation of V2a Gi neurons led mice to decelerate and change their heading direction towards the stimulated side. Similarly, frequent turning to the opposite side during locomotion was observed upon unilateral silencing of these neurons. Intriguingly, however, stimulation experiments in stationary animals painted a more complicated picture of V2a function than a simple asymmetric braking. For instance, reminiscent of earlier findings with a larger population of glutamatergic Gi neurons [11], unrestrained mice responded to unilateral V2a stimulation by horizontally reorienting their head and body even when at rest. With those movements prevented through head-fixing, the same stimulation protocol evoked deflection of the snout
SUPERIOR COLLICULUS Headlights Sensory integration & orienting vectors
MESENCEPHALIC LOCOMOTOR REGION Ignition & gas pedal Locomotion intiation & speed setting
LATERAL PARAGIGANTOCELLULAR NUCLEUS Spark plug & throttle valve Locomotion intiation relay & speed control
GIGANTOCELLULAR NUCLEUS Wheel & brake pedal Locomotion steering & termination
SPINAL CORD Engine Rhythm generation Coordinated control of flexor & extensor muscles within and across body parts F
E
Flexor and extensor half-centres Current Biology
Figure 1. Brainstem motor centres reimagined as an automobile. As shown by Usseglio et al. [1], the gigantocellular nucleus is analogous to the brakes and the steering wheel of locomotion, guided by superior colliculus. In parallel, the mesencephalic locomotor region (MLR) initiates, and sets the speed of, locomotion, functioning as both the ignition system and the gas pedal. Downstream of these, the spark plug and the throttle valve control the engine, much like the lateral paragigantocellular nucleus communicates information from the MLR to the spinal cord.
along the horizontal axis. Notably, these motor elements — snout deflection, head rotation, body reorientation — were evoked with distinct latencies, and occurred in the same temporal sequence as during self-generated changes in locomotor trajectory. As these movements were not necessarily accompanied by deceleration, this implicates the brainstem V2a neurons in orienting movements beyond those associated with left–right asymmetric activity of the limbs, and tentatively decouple their roles in steering and braking. How could such diverse motor outputs be generated by a single population of brainstem neurons? Usseglio et al. [1] reasoned that the population would require access to multiple motor circuits, and so mapped the axons of these neurons through selective expression of a fluorescent protein. They found dense innervation of regions involved in movements of the snout, whiskers, neck and hindlimb. But do all V2a Gi neurons have the same projection pattern and, presumably, function? The authors addressed this by using a series of retrograde tracing approaches targeted to the cervical and lumbar spinal cord
segments, controlling movements of the neck and hindlimb, respectively. This experiment uncovered subsets of V2a neurons that project to either cervical or lumbar levels, but very rarely both, showing that there are multiple projection-defined V2a Gi cell types. Stimulation of these individual neuron types revealed a remarkable division of orienting and locomotor behaviours. Unilateral stimulation of only the lumbarprojecting V2a neurons halted locomotion without changing movement trajectory, much like upon bilateral V2a stimulation in the brainstem [12]. Conversely, selective activation of the cervical-projecting V2a neurons resulted in head rotation and body reorientation, with no significant effect on locomotor speed. Considering the distinct behavioural specialisations of these V2a subpopulations and their additive effects during collective activation, it is tempting to imagine how dynamic mixing and matching of these separate pathways’ activities could result in a highly versatile controller employable in wide-ranging contexts. Like a Swiss army knife of motor coordination, this system could aid responses as diverse as whole-body freezing when under a threat,
Current Biology 30, R1413–R1441, December 7, 2020 R1419
ll a head rotation towards a familiar sound, and, indeed, a well-calibrated turn around the corner by a mouse chasing its meal. There are still many aspects of orienting movements that we do not understand. How, for example, does the nervous system learn to recruit these motor modules in a behaviourally relevant fashion? Or, what is the circuit logic linking V2a Gi neurons with the various spinal inter- and motor neurons that produce the behaviour? The study by Usseglio et al. [1] takes an important step to answering such questions around this important behaviour. REFERENCES , A., He rent, C., 1. Usseglio, G., Gatier, E., Heuze and Bouvier, J. (2020). Control of orienting movements and locomotion by projectiondefined subsets of brainstem V2a neurons. Curr. Biol. 30, 4665–4681. 2. Graham-Brown, T. (1911). The intrinsic factors in the act of progression in the mammal. Proc. R. Soc. Lond. B 84, 309–319.
Dispatches 3. Graham-Brown, T. (1914). On the nature of the fundamental activity of the nervous centres; together with an analysis of the conditioning of rhythmic activity in progression, and a theory of the evolution of function in the nervous system. J. Physiol. 48, 18–46.
10. Josset, N., Roussel, M., Lemieux, M., Lafrance-Zougba, D., Rastqar, A., and Bretzner, F. (2018). Distinct contributions of mesencephalic locomotor region nuclei to locomotor control in the freely behaving mouse. Curr. Biol. 28, 884–901.
4. Goulding, M. (2009). Circuits controlling vertebrate locomotion: moving in a new direction. Nat. Rev. Neurosci. 10, 507–518.
11. Capelli, P., Pivetta, C., Soledad Esposito, M., and Arber, S. (2017). Locomotor speed control circuits in the caudal brainstem. Nature 551, 373–377.
5. Jessell, T.M. (2000). Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1, 20–29. 6. Kiehn, O. (2016). Decoding the organization of spinal circuits that control locomotion. Nat. Rev. Neurosci. 17, 224–238. 7. Arber, S. (2011). Motor circuits in action: specification, connectivity, and function. Neuron 74, 975–989.
12. Bouvier, J., Caggiano, V., Leiras, R., Caldeira, V., Bellardita, C., Balueva, K., Fuchs, A., and Kiehn, O. (2015). Descending command neurons in the brainstem that halt locomotion. Cell 163, 1191–1203. 13. Gandhi, N.J., and Katnani, H.A. (2011). Motor functions of the superior colliculus. Annu. Rev. Neurosci. 34, 205–231.
8. Shik, M.L., and Orlovsky, G.N. (1976). Neurophysiology of locomotor automatism. Physiol. Rev. 56, 465–501.
14. Massulo, L., Mariotti, L., Alexandre, N., FreirePritchett, P., Boulanger, J., and Tripodi, M. (2019). Genetically defined functional modules for spatial orienting in the mouse superior colliculus. Curr. Biol. 29, 2892–2904.
9. Caggiano, V., Leiras, R., Goni-Erro, H., Masini, D., Bellardita, C., Bouvier, J., Caldeira, V., Fisone, G., and Kiehn, O. (2018). Midbrain circuits that set locomotor speed and gait selection. Nature 553, 455–460.
15. Cregg, J.M., Leiras, R., Montalant, A., Wanker, P., Wickersham, I.R., and Kiehn, O. (2020). Brainstem neurons that command mammalian locomotor asymmetries. Nat. Neurosci. 23, 730–740.
Plant Biology: Gynoecium Development with Style Stefan de Folter
cnico Nacional Unidad de Geno´mica Avanzada (UGA-LANGEBIO), Centro de Investigacio´n y de Estudios Avanzados del Instituto Polite xico (CINVESTAV-IPN), Km 9.6 Libramiento Norte, Carretera Irapuato-Leo´n, C.P. 36824 Irapuato, Me Correspondence: [email protected] https://doi.org/10.1016/j.cub.2020.10.040
The gynoecium is the female reproductive part of the flower and is essential for plant sexual reproduction. A new study shows a novel angiosperm-specific gene family that fine tunes the architecture of the stigma and style in Arabidopsis. Most plant species on earth are angiosperms, which produce flowers. Most flowers produce in their center a gynoecium or pistil, surrounded by the androecium or the stamens. Stamens produce pollen and the pistil produces ovules — these two components are the basis of sexual reproduction in plants. A rich diversity of floral structures, shapes and sizes is present in nature, as well as variations in the process of sexual reproduction. Although, generalizing, pollen grains land on the stigma of the pistil and germinate, and each pollen grain forms a pollen tube to bring its content to the egg cell inside the ovule to fertilize it
(Figure 1) [1–3]. Understanding these simple sounding events, which in reality are enormously complex, is of great interest to many. Many molecular insights come from the model plant Arabidopsis thaliana, which serves as a good genetic system to unravel the gene regulatory networks that guide androecium and gynoecium development [4–7], as well as the networks involved in pollen tube growth and male gametophyte (pollen) interaction with the gynoecium [1–3]. Focusing on the Arabidopsis gynoecium, we can divide the structure into three parts — from top to bottom, the stigma and style form the apical part, the
R1420 Current Biology 30, R1413–R1441, December 7, 2020 ª 2020 Elsevier Inc.
ovary with ovules inside forms the middle part, and the basal part is the gynophore that forms the connection with the mother plant (Figure 1). Various tissue types are present inside the gynoecium; one is called the transmitting tract tissue and produces extracellular matrix, which is a mixture of polysaccharides, glycoproteins, and glycolipids through which pollen tubes will grow when passing through the style and the ovary to reach the ovules [8–10]. Many transcription factors involved in gynoecium development have been identified over the last three decades by many labs [4,6,7,11]. Related to the apical