Nyctinasty

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Illustration of sleep movements in Medicago leaves, from Charles Darwin's The Power of Movement in Plants (1880) Fig139Movement of Plants.png
Illustration of sleep movements in Medicago leaves, from Charles Darwin's The Power of Movement in Plants (1880)

In plant biology, nyctinasty is the circadian rhythm-based nastic movement of higher plants in response to the onset of darkness, or a plant "sleeping". Nyctinastic movements are associated with diurnal light and temperature changes and controlled by the circadian clock. It has been argued that for plants that display foliar nyctinasty, it is a crucial mechanism for survival; however, most plants do not exhibit any nyctinastic movements. [1] Nyctinasty is found in a range of plant species and across xeric, mesic, and aquatic environments, suggesting that this singular behavior may serve a variety of evolutionary benefits. Examples are the closing of the petals of a flower at dusk and the sleep movements of the leaves of many legumes.

Contents

Physiology

Plants use phytochrome to detect red and far red light. Depending on which kind of light is absorbed, the protein can switch between a Pr state that absorbs red light and a Pfr state that absorbs far red light. Red light converts Pr to Pfr and far red light converts Pfr to Pr. Many plants use phytochrome to establish circadian cycles which influence the opening and closing of leaves associated with nyctastic movements. Anatomically, the movements are mediated by pulvini. Pulvinus cells are located at the base or apex of the petiole and the flux of water from the dorsal to ventral motor cells regulates leaf closure. This flux is in response to movement of potassium ions between pulvinus and surrounding tissue. Movement of potassium ions is connected to the concentration of Pfr or Pr. In Albizia julibrissin , longer darker periods, leading to low Pfr, result in a faster leaf opening. [2] In the SLEEPLESS mutation of Lotus japonicus , the pulvini are changed into petiole-like structures, rendering the plant incapable of closing its leaflets at night. [3] Non-pulvinar mediated movement is also possible and happens through differential cell division and growth on either side of the petiole, resulting in a bending motion within the leaves to the desired position. [4]

Leaf movement is also controlled by bioactive substances known as leaf opening or leaf closing factors. Several leaf-opening and leaf-closing factors have been characterized biochemically. [5] These factors differ among plants. Leaf closure and opening is mediated by the relative concentrations of leaf opening and closing factors in a plant. [6] Either the leaf opening or closing factor is a glycoside, which is inactivated by hydrolysis of the glycosidic bond via beta glucosidase. In Lespedeza cuneata the leaf opening factor, potassium lespedezate, is hydrolyzed to 4 hydroxy phenyl pyruvic acid. [7] In Phyllanthus urinaria , leaf closing factor Phyllanthurinolactone is hydrolyzed to its aglycon during the day. [8] Beta glucosidase activity is regulated via circadian rhythms.

Fluorescence studies have shown that the binding sites of leaf opening and closing factors are located on the surface of the motor cell. Shrinking and expansion of the motor cell in response to this chemical signal allows for leaf opening and closure. The binding of leaf opening and closing factors is specific to related plants. The leaf movement factor of Chamaecrista mimosoides (formerly Cassia mimosoides) was found to not bind to the motor cell of Albizia julibrissin . [9] The leaf movement factor of Albizia julibrissin similarly didn't bind to the motor cell of Chamaecrista mimosoides, but did bind to Albizia saman and Albizia lebbeck . [10]

Function

The functions of nyctinastic movement have yet to be conclusively identified, although several have been proposed. Minorsky hypothesized that nyctinastic behaviors are adaptive due to the plant being able to reduce its surface area during night time, which can lead to better temperature retention and also reduces night-time herbivory. [11] Minorsky specifically suggests a Tritrophic Hypothesis in which he considers the predators of herbivores in addition to the plants and herbivores themselves. By moving leaves up or down, herbivores become more visible to nocturnal predators in both a spatial and olfactory sense, increasing herbivore predation and subsequently decreasing damage to a plant's leaves. [1] Studies using mutant plants with a loss of function gene that results in petiole growth instead of pulvini found that these plants have less biomass and smaller leaf area than the wild type. This indicates nyctinastic movement may be beneficial toward plant growth. [12]

Charles Darwin believed that nyctinasty exists to reduce the risk of plants freezing. [13]

Nyctinasty may occur to protect the pollen, keeping pollen dry and intact during the nighttime when most pollinating insects are inactive. [14] Conversely, some flowers that are pollinated by moths or bats exhibit nyctinastic flower opening at night. [14]

History

The earliest recorded observation of this behavior in plants dates back to 324 BC when Androsthenes of Thasos, a companion to Alexander the Great, noted the opening and closing of tamarind tree leaves from day to night. [15] Carl Linnaeus (1729) proposed that this was the plants sleeping, but this idea has been widely contested.

Related Research Articles

<span class="mw-page-title-main">Circadian rhythm</span> Natural internal process that regulates the sleep-wake cycle

A circadian rhythm, or circadian cycle, is a natural oscillation that repeats roughly every 24 hours. Circadian rhythms can refer to any process that originates within an organism and responds to the environment. Circadian rhythms are regulated by a circadian clock whose primary function is to rhythmically co-ordinate biological processes so they occur at the correct time to maximise the fitness of an individual. Circadian rhythms have been widely observed in animals, plants, fungi and cyanobacteria and there is evidence that they evolved independently in each of these kingdoms of life.

<span class="mw-page-title-main">Plant physiology</span> Subdiscipline of botany

Plant physiology is a subdiscipline of botany concerned with the functioning, or physiology, of plants. Closely related fields include plant morphology, plant ecology, phytochemistry, cell biology, genetics, biophysics and molecular biology.

<span class="mw-page-title-main">Phytochrome</span> Protein used by plants, bacteria and fungi to detect light

Phytochromes are a class of photoreceptor proteins found in plants, bacteria and fungi. They respond to light in the red and far-red regions of the visible spectrum and can be classed as either Type I, which are activated by far-red light, or Type II that are activated by red light. Recent advances have suggested that phytochromes also act as temperature sensors, as warmer temperatures enhance their de-activation. All of these factors contribute to the plant's ability to germinate.

<span class="mw-page-title-main">Heliotropism</span> Motion of flowers or leaves to face the Sun

Heliotropism, a form of tropism, is the diurnal or seasonal motion of plant parts in response to the direction of the Sun.

In developmental biology, photomorphogenesis is light-mediated development, where plant growth patterns respond to the light spectrum. This is a completely separate process from photosynthesis where light is used as a source of energy. Phytochromes, cryptochromes, and phototropins are photochromic sensory receptors that restrict the photomorphogenic effect of light to the UV-A, UV-B, blue, and red portions of the electromagnetic spectrum.

<i>Mimosa pudica</i> Species of plant whose leaves fold inward and droop when touched or shaken

Mimosa pudica is a creeping annual or perennial flowering plant of the pea/legume family Fabaceae. It is often grown for its curiosity value: the sensitive compound leaves fold inward and droop when touched or shaken and re-open a few minutes later. Mimosa pudica is not a carnivorous plant. Mimosa pudica is well known for its rapid plant movement. Like a number of other plant species, it undergoes changes in leaf orientation termed "sleep" or nyctinastic movement. The foliage closes during darkness and reopens in light. This was first studied by French scientist Jean-Jacques d'Ortous In the UK it has gained the Royal Horticultural Society's Award of Garden Merit.

Thermotropism or thermotropic movement is the movement of an organism or a part of an organism in response to heat or changes from the environment's temperature. A common example is the curling of Rhododendron leaves in response to cold temperatures. Mimosa pudica also show thermotropism by the collapsing of leaf petioles leading to the folding of leaflets, when temperature drops.

Photoperiodism is the physiological reaction of organisms to the length of light or a dark period. It occurs in plants and animals. Plant photoperiodism can also be defined as the developmental responses of plants to the relative lengths of light and dark periods. They are classified under three groups according to the photoperiods: short-day plants, long-day plants, and day-neutral plants.

Shade avoidance is a set of responses that plants display when they are subjected to the shade of another plant. It often includes elongation, altered flowering time, increased apical dominance and altered partitioning of resources. This set of responses is collectively called the shade-avoidance syndrome (SAS).

Far-red light is a range of light at the extreme red end of the visible spectrum, just before infrared light. Usually regarded as the region between 700 and 750 nm wavelength, it is dimly visible to human eyes. It is largely reflected or transmitted by plants because of the absorbance spectrum of chlorophyll, and it is perceived by the plant photoreceptor phytochrome. However, some organisms can use it as a source of energy in photosynthesis. Far-red light also is used for vision by certain organisms such as some species of deep-sea fishes and mantis shrimp.

<span class="mw-page-title-main">Nastic movements</span> Undirected movement in response to external stimuli

In biology, nastic movements are non-directional responses to stimuli, and are usually associated with plants. The movement can be due to changes in turgor. Decrease in turgor pressure causes shrinkage, while increase in turgor pressure brings about swelling. Nastic movements differ from tropic movements in that the direction of tropic responses depends on the direction of the stimulus, whereas the direction of nastic movements is independent of the stimulus's position. The tropic movement is growth movement but nastic movement may or may not be growth movement. The rate or frequency of these responses increases as intensity of the stimulus increases. An example of such a response is the opening and closing of flowers, movement of euglena, chlamydomonas towards the source of light. They are named with the suffix "-nasty" and have prefixes that depend on the stimuli:

<span class="mw-page-title-main">Thigmonasty</span> Undirected movement in response to touch or vibration

In biology, thigmonasty or seismonasty is the nastic (non-directional) response of a plant or fungus to touch or vibration. Conspicuous examples of thigmonasty include many species in the leguminous subfamily Mimosoideae, active carnivorous plants such as Dionaea and a wide range of pollination mechanisms.

<span class="mw-page-title-main">Plant perception (physiology)</span> Plants interaction to environment

Plant perception is the ability of plants to sense and respond to the environment by adjusting their morphology and physiology. Botanical research has revealed that plants are capable of reacting to a broad range of stimuli, including chemicals, gravity, light, moisture, infections, temperature, oxygen and carbon dioxide concentrations, parasite infestation, disease, physical disruption, sound, and touch. The scientific study of plant perception is informed by numerous disciplines, such as plant physiology, ecology, and molecular biology.

The repressilator is a genetic regulatory network consisting of at least one feedback loop with at least three genes, each expressing a protein that represses the next gene in the loop. In biological research, repressilators have been used to build cellular models and understand cell function. There are both artificial and naturally-occurring repressilators. Recently, the naturally-occurring repressilator clock gene circuit in Arabidopsis thaliana and mammalian systems have been studied.

Photoreceptor proteins are light-sensitive proteins involved in the sensing and response to light in a variety of organisms. Some examples are rhodopsin in the photoreceptor cells of the vertebrate retina, phytochrome in plants, and bacteriorhodopsin and bacteriophytochromes in some bacteria. They mediate light responses as varied as visual perception, phototropism and phototaxis, as well as responses to light-dark cycles such as circadian rhythm and other photoperiodisms including control of flowering times in plants and mating seasons in animals.

<span class="mw-page-title-main">Pulvinus</span> Swollen or thickened leaf base

A pulvinus is a joint-like thickening at the base of a plant leaf or leaflet that facilitates growth-independent movement. Pulvini are common, for example, in members of the bean family Fabaceae (Leguminosae) and the prayer plant family Marantaceae.

<span class="mw-page-title-main">Chelidonic acid</span> Chemical compound

Chelidonic acid is a heterocyclic organic acid with a pyran skeleton.

<span class="mw-page-title-main">Ruth Lyttle Satter</span> American botanist

Ruth Lyttle Satter was an American botanist best known for her work on circadian leaf movement.

Paraheliotropism refers to the phenomenon in which plants orient their leaves parallel to incoming rays of light, usually as a means of minimizing excess light absorption. Excess light absorption can cause a variety of physiological problems for plants, including overheating, dehydration, loss of turgor, photoinhibition, photo-oxidation, and photorespiration, so paraheliotropism can be viewed as an advantageous behavior in high light environments. Not all plants exhibit this behavior, but it has developed in multiple lineages.

Elaine Munsey Tobin is a professor of molecular, cell, and developmental biology at the University of California, Los Angeles (UCLA). Tobin is recognized as a Pioneer Member of the American Society of Plant Biologists (ASPB).

References

  1. 1 2 Minorsky, Peter V. (July 2018). "The functions of foliar nyctinasty: a review and hypothesis". Biological Reviews of the Cambridge Philosophical Society. 94 (1): 216–229. doi: 10.1111/brv.12444 . PMC   7379275 . PMID   29998471.
  2. ↑ Satter, R. L.; Applewhite, P. B.; Galston, A. W. (1 October 1972). "Phytochrome-controlled Nyctinasty in Albizzia julibrissin: V. Evidence against Acetylcholine Participation". Plant Physiology. 50 (4): 523–525. doi:10.1104/pp.50.4.523. PMC   366182 . PMID   16658209.
  3. ↑ Kawaguchi M (2003). "SLEEPLESS, a gene conferring nyctinastic movement in legume". J. Plant Res. 116 (2): 151–154. doi:10.1007/s10265-003-0079-5. PMID   12736786. S2CID   21112729.
  4. ↑ Wetherell, D. F. (1990). "Leaf movements in plants without pulvini". The Pulvinus Motor: 72–78.
  5. ↑ Ueda M, Nakamura Y (2007). "Chemical basis of plant leaf movement". Plant Cell Physiol. 48 (7): 900–907. doi:10.1093/pcp/pcm060. PMID   17566057.
  6. ↑ Ohnuki, Takashi; Ueda, Minoru; Yamamura, Shosuke (October 1998). "Molecular mechanism of the control of nyctinastic leaf-movement in Lespedeza cuneata G. Don". Tetrahedron. 54 (40): 12173–12184. doi:10.1016/S0040-4020(98)00747-9.
  7. ↑ Ueda, Minoru; Yamamura, Shosuke (17 April 2000). "Chemistry and Biology of Plant Leaf Movements". Angewandte Chemie International Edition. 39 (8): 1400–1414. doi:10.1002/(SICI)1521-3773(20000417)39:8<1400::AID-ANIE1400>3.0.CO;2-Z. PMID   10777626.
  8. ↑ Ueda, Minoru; Asano, Miho; Sawai, Yoshiyuki; Yamamura, Shosuke (April 1999). "Leaf-movement factors of nyctinastic plant, Phyllanthus urinaria L.; the universal mechanism for the regulation of nyctinastic leaf-movement". Tetrahedron. 55 (18): 5781–5792. doi:10.1016/S0040-4020(99)00236-7.
  9. ↑ Sugimoto, Takanori; Wada, Yoko; Yamamura, Shosuke; Ueda, Minoru (December 2001). "Fluorescence study on the nyctinasty of Cassia mimosoides L. using novel fluorescence-labeled probe compounds". Tetrahedron. 57 (49): 9817–9825. doi:10.1016/S0040-4020(01)00999-1.
  10. ↑ Lattanzio, Vincenzo; Escribano-Bailon, Maria Teresa; Santos-Buelga, Celestino (2010). Recent advances in polyphenol research. Oxford: Wiley-Blackwell. ISBN   978-1405193993.
  11. ↑ Minorsky, Peter V. (2018-07-11). "The functions of foliar nyctinasty: a review and hypothesis". Biological Reviews of the Cambridge Philosophical Society. 94 (1): 216–229. doi: 10.1111/brv.12444 . ISSN   1469-185X. PMC   7379275 . PMID   29998471.
  12. ↑ Zhou, Chuanen; Han, Lu; Fu, Chunxiang; Chai, Maofeng; Zhang, Wenzheng; Li, Guifen; Tang, Yuhong; Wang, Zeng-Yu (October 2012). "Identification and characterization of petiolule- like pulvinus mutants with abolished nyctinastic leaf movement in the model legume Medicago truncatula". New Phytologist. 196 (1): 92–100. doi:10.1111/j.1469-8137.2012.04268.x. PMC   3504090 . PMID   22891817.
  13. ↑ Why Do Flowers Close Up at Night? Elizabeth Palermo, Live Science, May 22, 2013
  14. 1 2 Why do poppy flowers open in the morning and close at night? BBC Science, Luis Villazon
  15. ↑ Otsuka, Kuniaki (18 March 2016). Chronomics and Continuous Ambulatory Blood Pressure Monitoring: Vascular Chronomics: From 7-Day/24-Hour to Lifelong Monitoring. Springer. pp. ix. ISBN   978-4431546306.
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