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Genetic Basis of the “Sleeping Leaves” Revealed

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Genetic Basis of the “Sleeping Leaves” Revealed COMMENTARY Genetic basis of the “sleeping leaves” revealed Millán Cortizo and Patrick Laufs1 Institut National de la Recherche Agronomique, Unité Mixte de Recherche 1318, and AgroParisTech, Institut Jean-Pierre Bourgin, F-78000 Versailles, France ike most animals, plants also sleep at night, or at least some of them. L For instance, the flowers of many species, such as crocus, tulip, and morning glory, are open during the day or part of the day and close at night. Based on such observations, in 1751, the Swedish botanist Carl von Linné suggested com- bining several plant species in which the flowers open or close at specific and different times of the day to build a “Horologium Florae” (flower clock) that would accurately and colorfully predict time. Such daily movements of plants are not limited to flowers. In his book entitled The Power of Movement in Plants, Darwin (1880) described many examples of “sleep movements of leaves” and provided a “List of Genera, including species the leaves of which sleep” (1). Among these, he noted that the legume family “includes many more genera with sleeping species than all the other families put together.” He also described a specialized organ, called a joint, cushion, or pulvinus responsible for such movement (1). In PNAS, Chen et al. (2) identify the genetic determinant for the formation of these pulvini in three legumes: Fig. 1. Leaf of M. arabica (A) shows a detail of the pulvinus (B) and the extensor cells (C). (D) Schema Pisum sativum (pea), Medicago truncatula depicts nyctinasty in M. truncatula WT and elp1 mutant. (barrel medic), and Lotus japonicus. Contrary to intuition, plants are capable are surrounded by parenchyma. The outer There is abundant literature describing of moving in response to environmental cells of the parenchyma, called the motor the anatomy of the pulvinus and the stimuli. This movement is achieved cells, undergo water-driven volume physiology and biomechanics of nyctinastic either through irreversible differential changes and are the ultimate effectors of movements in legumes (e.g., reviewed in growth or through reversible changes movement. Motor cells are distributed 3). However, nothing was known about in turgor. An example of differential into two positionally and functionally the development of this organ, probably growth is the growth toward a light source opposed regions: extensor and flexor. because Arabidopsis lacks an equivalent (phototropism) observed in the majority Extensors cells are located in the upper of plant shoots. Tropisms are plant structure. The report of Chen et al. (2) side of the organ, whereas flexors are fi fi movements induced by directional stimuli, starts to ll this void through the identi - located in the lower side. During leaf cation of the genetic factor that determi- such as light or gravity. In addition, plants fl can move in response to nondirectional opening, lea ets move downward by the nates pulvinus formation in legumes. This simultaneous increase of turgor pressure collaborative work between teams of three factors, such as humidity or contact. These fl movements are called nastic responses. in extensor and decrease in exor cells. different continents working on three Nyctinasty, the proper name for the “sleep During closing, the inverse occurs, exten- different legume models nicely illustrates fl movements of leaves” is a well-known sor cells shrink, and exor cells swell, what can be achieved when the use of fl example of a nastic response. In this case, moving lea ets upward (3). These turgor large, well-established collections of plants close up their leaves and petals in changes in the motor cells are caused by mutants meets the most advanced plant response to the onset of darkness. Because ion movements followed by massive water molecular genetic approaches. fl it is a rather fast response, it does not ux across the plasma membrane. Swelling The whole story started more than involve differential growth but changes in is caused by proton pump-driven accu- 50 y ago, when Stig Blixt identified a pea + − cellular turgor. mulation in the cytoplasm of K and Cl . mutant he called petiolulatus in which fo- The pulvinus is the organ responsible This increase in solute concentration low- liar pulvini are replaced by petiolules (6). for the nyctinastic leaf movement. It is ers water potential inside the cell, and thus a specialized structure located at the base drives the entrance of water in the cell. of the petiole of leaves or the petiolule of Shrinking is caused by a passive leaking of Author contributions: M.C. and P.L. wrote the paper. leaflets in the case of compound leaves solutes that is accompanied by water loss. The authors declare no conflict of interest. (Fig. 1A). In the pulvinus (Fig. 1 B and C), It is currently accepted that the osmotic See companion article 10.1073/pnas.1204566109. the central vascular bundles and the volume changes of motor cells are analo- 1To whom correspondence should be addressed. E-mail: supporting tissues (often, sclerenchyma) gous to those of stomatal guard cells (4, 5). [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1209532109 PNAS Early Edition | 1of2 Downloaded by guest on September 23, 2021 This mutant was later renamed apulvinic epidermal cells (2). This change in the cell a CX2CX6CX3C motif and a 30-aa-long (apu), according to another mutant type and expansion pattern may explain domain predicted to form a coiled coil independently found in 1979 by D. M. the elongated petiolule phenotype of the reminiscent of a leucine zipper that may Harvey (7). Although pea is a very nice elp1/apu/slp mutants. Conversely, over- be involved in interaction with LBD or model for performing genetic analyses, it expression of ELP1 in M. truncatula leads other proteins. The LBD family contains is somehow more difficult to clone genes to dwarf plants, with shorter petioles and 43 members in either Arabidopsis or from this species, and this probably ex- leaf rachises, which correlates with a maize, and the LOB domain accounts for plains why no further progress toward this reduction in the size of the epidermal cells the specificity of the members of this has been made. In 2003, Kawaguchi (8) family (11). Close homologs of the ELP1/ identified from a population of chemically Formation of the APU/SLP1 genes can been found in other mutagenized L. japonicus a mutant that species in which no similar pulvinus are could not close its leaflets at night because pulvinus in legumes is observed, such as maize and Arabidopsis. of an absence of differentiated pulvini, Some of them, like LOB in Arabidopsis, which was therefore called sleepless (slp). likely to be regulated by have been implicated in the establishment Again, cloning the SLP gene through fine of the frontiers between meristem and mapping was not an easy task. Finally, a conserved genetic lateral organs (10). Similarly, ELP1 is a similar mutant called elongated petiolule1 expressed very early on in the basal region (elp1) with pulvini replaced by longer network orchestrated of the leaflet, the region that will later petiolule-like structures was described in differentiate into the pulvinus, in a fashion M. truncatula. In this mutant, leaves by the ELP1/APU/SLP1 reminiscent of a frontier gene (2). Over- remain open at night (2) (Fig. 1D). The expression of ELP1, like overexpression of fi combination of ne genetic mapping of genes. LOB, leads to dwarf plants (10), suggest- fi the elp1 mutation with the identi cation of ing that one common function of these fl the anking sequences of newly generated genes would be to control cell expansion. in the transgenic lines. Interestingly, in elp1 alleles through the insertion of a Therefore, ELP1 may share some func- fi these plants, the small epidermal cells of retrotransposon allowed the identi ca- tions with related LBD genes from other the petiole and rachis show some convo- tion of the ELP1 gene. From this, the species, although retaining species- and fi lution at their surface reminiscent of APU and SLP genes could be identi ed as even organ-specific roles, as shown by the pulvinus cells, indicating that ELP1 may ELP1 orthologs bearing mutations in the differential response of M. truncatula be sufficient to some degree for the respective pea and L. japonicus mutants. rachis and petiolule to ELP1 over- acquisition of the pulvinus identity. Con- Therefore, the work of Chen et al. (2) expression (2). Further comparative anal- firmation of this hypothesis awaits further reveals that the formation of the pulvinus ysis of the role of these genes between identification of molecular markers of in legumes is likely to be regulated by different species, including the elucidation the pulvinus. a conserved genetic network orchestrated of the downstream genetic network, will ELP1/APU/SLP1 codes for nuclear- by the ELP1/APU/SLP1 genes. Identi- be necessary to understand how ELP1 fi localized proteins belonging to the plant- cation of these genes also provides triggers pulvinus differentiation. By iden- specific LATERAL ORGAN BOUND- a straightforward way to test whether tifying a key determinant of the formation pulvinus formation in more distantly ARIES domain (LBD) transcription factor of a specialized plant structure, the work related species is controlled by the same family (2). In the past years, LBD mem- of Chen et al. (2) provides a unique op- genetic determinants. bers have been shown to have essential portunity to understand better the genetic What do the mutant phenotypes tell us regulatory functions for the development basis and evolution of the diversity observed about ELP1/APU/SLP functions? In the of plant lateral organs (9, 10). LBD pro- in plants. absence of these genes, the small, iso- teins have a characteristic N-terminal lat- eral organ boundaries (LOB) domain that diametric, epidermal pulvinus cells with ACKNOWLEDGMENTS.
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