Chlororespiration

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Chlororespiration basics Chlororespiration basics.jpg
Chlororespiration basics

Chlororespiration is a respiratory process that takes place within plants. Inside plant cells there is an organelle called the chloroplast which is surrounded by the thylakoid membrane. This membrane contains an enzyme called NAD(P)H dehydrogenase which transfers electrons in a linear chain to oxygen molecules. [1] This electron transport chain (ETC) within the chloroplast also interacts with those in the mitochondria where respiration takes place. [2] Photosynthesis is also a process that Chlororespiration interacts with. [2] If photosynthesis is inhibited by environmental stressors like water deficit, increased heat, and/or increased/decreased light exposure, or even chilling stress then chlororespiration is one of the crucial ways that plants use to compensate for chemical energy synthesis. [3] [4] [5]

Contents

Chlororespiration – the latest model

A diagram depicting an early understanding of the process of chlororespiration Initial model of chlororespiration.jpg
A diagram depicting an early understanding of the process of chlororespiration

Initially, the presence of chlororespiration as a legitimate respiratory process in plants was heavily doubted. However, experimentation on Chlamydomonas reinhardtii, discovered Plastoquinone (PQ) to be a redox carrier. [2] The role of this redox carrier is to transport electrons from the NAD(P)H enzyme to oxygen molecules on the thylakoid membrane. [6] Using this cyclic electron chain around photosystem one (PS I), chlororespiration compensates for the lack of light. This cyclic pathway also allows electrons to re-enter the PQ pool through NAD(P)H enzyme activity and production, which is then used to supply ATP molecules (energy) to plant cells. [7]


A diagram depicting newly discovered molecules (PTOX and the NDH complex) as part of the chlororespiratory process in higher order plants like Rosa Meillandina. Latest understanding of chlororespiration (2002).jpg
A diagram depicting newly discovered molecules (PTOX and the NDH complex) as part of the chlororespiratory process in higher order plants like RosaMeillandina.

In the year 2002, the discovery of the molecules; plastid terminal oxidase (PTOX) and NDH complexes have revolutionised the concept of chlororespiration. [2] Using evidence from experimentation on the plant species Rosa Meillandina, this latest model observes the role of PTOX to be an enzyme that prevents the PQ pool from over-reducing, by stimulating its reoxidation. [4] Whereas, the NDH complexes are responsible for providing a gateway for electrons to form an ETC. [4] The presence of such molecules are apparent in the non-appressed thylakoid membranes of higher order plants like Rosa Meillandina. [5] [2] [3]

The relation between chlororespiration, photosynthesis and respiration

Chlamydomonas- a species in which chlororespiration, photosynthesis and respiration occur Chlamydomonas ( klmydwmwns).jpg
Chlamydomonas- a species in which chlororespiration, photosynthesis and respiration occur

Experimentation with respiratory oxidase inhibitors (for instance, cyanide) on unicellular algae has revealed interactive pathways to be present between chloroplasts and mitochondria. Metabolic pathways responsible for photosynthesis are present in chloroplasts, whereas respiratory metabolic pathways are present in mitochondria. In these pathways, metabolic carriers (like phosphate) exchange NAD(P)H molecules between photosynthetic and respiratory ETCs. [2] Evidence using mass spectrometry on algae and photosynthetic mutants of Chlamydomonas, discovered that oxygen molecules were also being exchanged between photosynthetic and chlororespiratory ETCs. [6] The mutant Chlamydomonas alga species, lacks photosystems one and two (PS I and PS II), so when the alga underwent flash-induced PS I activity, it resulted in no effect on mitochondrial pathways of respiration. Instead, this flash-induced PS I activity caused an exchange between photosynthetic and chlororespiratory ETCs, which was observed using polarography. [6] This flash of PS I activity is triggered by an over-reduction of the PQ pool and/or lack of the pyridine nucleotide in the thylakoid membrane. A reduction in such molecules then stimulates NADPH and PTOX molecules to trigger chlororespiratory pathways. [6] [2]

Furthermore, in the absence of light (and thus photosynthesis), chlororespiration plays an integral role in enabling metabolic pathways to compensate for chemical energy synthesis. [2] This is achieved through the oxidation of stromal compounds, which increases the PQ pool and allows for the chlororespiratory ETC to take place. [2] [6]

Stimulation of chlororespiration

Heat and light as stimulants

Quiles' experiment

Oat plants Green oat field.jpg
Oat plants

An experiment on oat plants by scientist Maria Quiles, revealed that extreme light intensity can inhibit photosynthesis and result in the lack of PS II activity. [4] This reduction leads to an increase in NAD(P)H and PTOX levels which then causes the stimulation of chlororespiration. [4]

Oat leaves were incubated and Chlorophyll fluorescence emission was used to examine the effect of extreme light intensity. [4] As the emission of the Chlorophyll fluorescence increased the PQ pool decreased. This stimulated the cyclic electron flow, causing NAD(P)H and PTOX levels to ultimately incline and initiate the process of chlororespiration within the thylakoid membrane of oat plants. [4]

The effect of adding n-propyl gallate to the incubated leaves was also observed. N-propyl gallate is a molecule that helps distinguish between PQ reduction and oxidation activities by inhibiting PTOX. [8] Quiles noted an increase in chlorophyll fluorescence inside the thylakoid membrane of plant cells, after the addition of n-propyl gallate. [4] The result led to the stimulation of the NAD(P)H enzyme and its cyclic pathway; causing a continuous increase in chlorophyll fluorescence levels within the oat. [4]

Quiles' conclusion

After comparing the metabolic responses between oat plants under an average light intensity to that of oat plants under extreme light intensity, Quiles noted that the amount of PS II produced was of a lower amount in the leaves that underwent chlororespiration in extreme light. [4] Whereas higher levels of PS II were yielded by those leaves that underwent average light intensity. A higher of PS II is more efficient for chemical energy synthesis and thus for a plant's survival. [4] Quiles indicates that although the chlororespiratory pathway is less efficient, it still serves as a back-up response for energy production in plants. [4] Ultimately, Quiles concluded that the intense light on oat plants had caused PS II levels to reduce and thus, initiate an influx of gate-way (NAD(P)H) proteins to start the process of chlororespiration. [4]

Drought as a stimulant

Paredes' and Quiles' experiment

Rosa Meillandina Rose Brilliant Meillandina bara buririanto meiandeina (8082922764).jpg
Rosa Meillandina

Scientists Miriam Paredes and Maria Quiles led an investigation on the plant species Rosa Meillandina, and its metabolic response to water deficit. [3] They noted how limited water irrigation can cause a reduction in PS II levels, which then results in the inhibition of photosynthesis. Paredes and Quiles also noticed the increase in chlororespiration activity as a protective mechanism for the lack of photosynthesis. [3]

In the experiment, the plants in water deficit were analysed with fluorescence imaging technique. This form of analysis detected increased levels of PTOX, and NAD(P)H activity within the plant. [3] An increase in these two molecules led to the initiation of chlororespiration. [3]

N-propyl gallate was also added to these water deficit plants. The effect resulted in increased chlorophyll fluorescence levels. [3] Quiles recorded a similar outcome in the same species of plants that went under intense light. [4] This increase in chlorophyll fluorescence is attributed to the influx of NAD(P)H in the thylakoid membrane. [3] Which then led to an increase in the by-product, hydrogen peroxide, inside the thylakoid membrane. [3] [4]

Paredes' and Quiles' conclusion

Paredes and Quiles concluded that chloroplasts under stress from water deficit rely on processes like the opening of stomata to disperse excess heat accumulated via metabolic processes within plant cells. [3] These metabolic processes are responsible for chemical energy synthesis that can be achieved via chlororespiratory ETCs when a reduction in photosynthesis activity is evident. [3]

Darkness as a stimulant

Gasulla's, Casano's and Guéra's experiment

Scientists Francisco Gasulla, Leonardo Casano and Alfredo Guéra, observed the lichen's metabolic response when placed in dark conditions. [8] The light harvesting complex (LHC) inside the chloroplasts of Lichen is activated when subjected to darkness. [8] Gasulla, Casano and Guéra, noticed that this increase in LHC activity caused PS II and the PQ pool within lichen to decrease, indicating the initiation of chlororespiration. [8]

Immunodetection analysis was used to determine the amount of LHC molecules inside lichen in a dark environment, and a luminous environment. By determining the amount of LHC within the chloroplast, scientists were able to notice the reduction in PS II activity. This reduction was caused by a loss in excitation energy in the PS II ETC, which then stimulated an incline in chlororespiratory pathways. Gasulla, Casano and Guéra, gathered this result, when both light-adapted and dark-adapted lichen were placed in darkness. They found that the level of LHC molecules in dark-adapted lichen had doubled compared to light adapted lichen. [8] It was also noted that the chlororespiratory ETCs were triggered at a much earlier time in dark-adapted lichen, than compared to light-adapted lichen. [8] This resulted in a faster metabolic rate and chemical synthesis response in dark-adapted lichen due to chlororespiration. [8]

Gasulla's, Casano's and Guéra's conclusion

Gasulla, Casano and Guéra, concluded that the longer the lichen are subjected to darkness, the quicker the chlororespiratory pathways can begin. [8] This is due to the fast depletion of PTOX molecules which reduce the PQ pool. [8] These events then stimulate chlororespiratory ETCs into an ongoing loop until the lichen are placed in a luminous environment. [8]

They also derived LHC to be another indicator for chlororespiration. [8] When LHC concentrations inside the chloroplast increased, PS II activity decreased due to loss in ETC activity. [8] This reduction then stimulated chlororespiratory activity to compensate for chemical energy synthesis. [8]

Lichen Flavoparmelia caperata - lichen - Caperatflechte.jpg
Lichen

Chilling stress as a stimulant

Segura's and Quiles' experiment

An experiment observing chilling stress on the tropical plant species, Spathiphyllum wallisii by scientists Maria Segura and Maria Quiles, showcased varying responses by chlororespiratory pathways when different parts of the plant were chilled at 10 degrees Celsius. [9]

Spathiphyllum wallisii Spathiphyllum wallisii (2).JPG
Spathiphyllum wallisii

Segura and Quiles noticed that when the roots of the plant were subjected to low temperatures (10 degrees Celsius), the level of chlororespiratory molecules (NADPH and PTOX) slightly varied when compared to the level of NADPH and PTOX within the controlled plant. [9] However, when the stem alone was cooled at 10 degrees Celsius, then the molecules NADPH, NDH and PTOX increased in amount as a result of reduced PS I activity. [9] Segura and Quiles then compared this result, by subjecting only the leaves of the plant to 10 degrees Celsius. [9] They noticed that this had caused the PS II activity to stop, and thus inhibit the process of photosynthesis. [9] The lack in photosynthetic activity, in combination with the incline in NADPH and PTOX molecules, then triggered chlororespiratory pathways to begin chemical energy synthesis. [9]

Furthermore, Segura and Quiles also noted that the simultaneous chilling of the leaves and heating of the roots (whilst the plant is under illumination), can cause the slowing and eventual inhibition of the ETC in PS II. [9] This then led to an over-reduction in the PQ pool., which ultimately stimulated chlororespiration. [9]

Segura and Quiles utilised the Fluorescence imaging technique to determine the level of photosynthetic activity in the leaves of the plants. By discerning the percentage of photosynthesis efficiency, Segura and Quiles were able to determine the likelihood of triggering chlororespiratory pathways. [9] They noticed that the percentage of photosynthesis efficiency remained high in test subjects where:

  • only the leaves were chilled
  • only the stem was chilled
  • only the roots were chilled [9]

This high percentage of photosynthesis efficiency meant that the chances of chlororespiration taking place are slim. [9] However, this was not true for the plant that underwent both stem chilling at 10 degrees Celsius and root heating at 24 degrees Celsius. [9] The photosynthesis efficiency of this test subject was significantly lower when compared to the experimental control. [9] This also indicated the inhibition of PS II activity which then caused chlororespiration to begin. [9]

Segura and Quiles also used an immunoblot analysis to deduce the effect of varying temperatures on different parts of the plant. Specifically, the immunoblot measures the amount of PTOX and NDH complex accumulated within the thylakoid membrane of the chloroplast organelle. [9] An increase in NDH complex was evident in the plant where the stem was chilled at 10 degrees Celsius and the root heated at 24 degrees Celsius. [9] Chlororespiration was stimulated in this plant. [9] Dissimilarly, the immunoblot analysis detected no variation in the levels NDH complex and PTOX molecules in test subjects where:

  • only the leaves were chilled
  • only the stem was chilled
  • only the roots were chilled [9]

These test subjects had similar concentrations of NDH and PTOX when compared to the concentration of NDH complex and PTOX molecules within the experimental control. [8] [9]

Segura's and Quiles' conclusion

Segura and Quiles concluded that chilling stress only induces chlororespiration when the stem is significantly cool and the roots are simultaneously warmer compared to the average Spathiphyllum wallisii in controlled conditions. [9] Segura and Quiles notice that PS II is present in chloroplast, (which is lacking in roots), thus by chilling the stem (which contains chloroplast), PS II ETCs can then be inhibited to trigger a reduction in PQ pool and as a result, chlororespiration. [9]

Importance of chlororespiration

Although chlororespiration is not as efficient as photosynthesis in producing energy, [9] its significance its attributed to its role as a survival adaptation for plants when placed in conditions lacking light [8] and water [3] or if placed in uncomfortable temperatures [9] [4] (note: optimum temperatures vary across different plant species). [9] Additionally, Cournac and Peltier noticed that chlororespiratory ETCs play a role in balancing electron flow across respiratory and photosynthetic ETCs. [2] This helps maintain water balance and regulate the plant's internal temperature. [2]

Related Research Articles

<span class="mw-page-title-main">Chloroplast</span> Plant organelle that conducts photosynthesis

A chloroplast is a type of membrane-bound organelle known as a plastid that conducts photosynthesis mostly in plant and algal cells. The photosynthetic pigment chlorophyll captures the energy from sunlight, converts it, and stores it in the energy-storage molecules ATP and NADPH while freeing oxygen from water in the cells. The ATP and NADPH is then used to make organic molecules from carbon dioxide in a process known as the Calvin cycle. Chloroplasts carry out a number of other functions, including fatty acid synthesis, amino acid synthesis, and the immune response in plants. The number of chloroplasts per cell varies from one, in unicellular algae, up to 100 in plants like Arabidopsis and wheat.

<span class="mw-page-title-main">Chlorophyll</span> Green pigments found in plants, algae and bacteria

Chlorophyll is any of several related green pigments found in cyanobacteria and in the chloroplasts of algae and plants. Its name is derived from the Greek words χλωρός, khloros and φύλλον, phyllon ("leaf"). Chlorophyll allow plants to absorb energy from light.

<span class="mw-page-title-main">Photosynthesis</span> Biological process to convert light into chemical energy

Photosynthesis is a process used by plants and other organisms to convert light energy into chemical energy that, through cellular respiration, can later be released to fuel the organism's activities. Some of this chemical energy is stored in carbohydrate molecules, such as sugars and starches, which are synthesized from carbon dioxide and water – hence the name photosynthesis, from the Greek phōs, "light", and synthesis, "putting together". Most plants, algae, and cyanobacteria perform photosynthesis; such organisms are called photoautotrophs. Photosynthesis is largely responsible for producing and maintaining the oxygen content of the Earth's atmosphere, and supplies most of the energy necessary for life on Earth.

<span class="mw-page-title-main">Thylakoid</span> Membrane enclosed compartments in chloroplasts and cyanobacteria

Thylakoids are membrane-bound compartments inside chloroplasts and cyanobacteria. They are the site of the light-dependent reactions of photosynthesis. Thylakoids consist of a thylakoid membrane surrounding a thylakoid lumen. Chloroplast thylakoids frequently form stacks of disks referred to as grana. Grana are connected by intergranal/stromal thylakoids, which join granum stacks together as a single functional compartment.

<span class="mw-page-title-main">Magnesium in biology</span> Use of Magnesium by organisms

Magnesium is an essential element in biological systems. Magnesium occurs typically as the Mg2+ ion. It is an essential mineral nutrient (i.e., element) for life and is present in every cell type in every organism. For example, adenosine triphosphate (ATP), the main source of energy in cells, must bind to a magnesium ion in order to be biologically active. What is called ATP is often actually Mg-ATP. As such, magnesium plays a role in the stability of all polyphosphate compounds in the cells, including those associated with the synthesis of DNA and RNA.

Photobiology is the scientific study of the beneficial and harmful interactions of light in living organisms. The field includes the study of photophysics, photochemistry, photosynthesis, photomorphogenesis, visual processing, circadian rhythms, photomovement, bioluminescence, and ultraviolet radiation effects.

<span class="mw-page-title-main">Plastoquinone</span> Molecule which moves electron in photosynthesis

Plastoquinone (PQ) is an isoprenoid quinone molecule involved in the electron transport chain in the light-dependent reactions of photosynthesis. The most common form of plastoquinone, known as PQ-A or PQ-9, is a 2,3-dimethyl-1,4-benzoquinone molecule with a side chain of nine isoprenyl units. There are other forms of plastoquinone, such as ones with shorter side chains like PQ-3 as well as analogs such as PQ-B, PQ-C, and PQ-D, which differ in their side chains. The benzoquinone and isoprenyl units are both nonpolar, anchoring the molecule within the inner section of a lipid bilayer, where the hydrophobic tails are usually found.

<span class="mw-page-title-main">Photosystem</span>

Photosystems are functional and structural units of protein complexes involved in photosynthesis. Together they carry out the primary photochemistry of photosynthesis: the absorption of light and the transfer of energy and electrons. Photosystems are found in the thylakoid membranes of plants, algae, and cyanobacteria. These membranes are located inside the chloroplasts of plants and algae, and in the cytoplasmic membrane of photosynthetic bacteria. There are two kinds of photosystems: PSI and PSII.

Chlorophyll <i>a</i> Chemical compound

Chlorophyll a is a specific form of chlorophyll used in oxygenic photosynthesis. It absorbs most energy from wavelengths of violet-blue and orange-red light, and it is a poor absorber of green and near-green portions of the spectrum. Chlorophyll does not reflect light but chlorophyll-containing tissues appear green because green light is diffusively reflected by structures like cell walls. This photosynthetic pigment is essential for photosynthesis in eukaryotes, cyanobacteria and prochlorophytes because of its role as primary electron donor in the electron transport chain. Chlorophyll a also transfers resonance energy in the antenna complex, ending in the reaction center where specific chlorophylls P680 and P700 are located.

<span class="mw-page-title-main">Photophosphorylation</span>

In the process of photosynthesis, the phosphorylation of ADP to form ATP using the energy of sunlight is called photophosphorylation. Cyclic photophosphorylation occurs in both aerobic and anaerobic conditions, driven by the main primary source of energy available to living organisms, which is sunlight. All organisms produce a phosphate compound, ATP, which is the universal energy currency of life. In photophosphorylation, light energy is used to pump protons across a biological membrane, mediated by flow of electrons through an electron transport chain. This stores energy in a proton gradient. As the protons flow back through an enzyme called ATP synthase, ATP is generated from ADP and inorganic phosphate. ATP is essential in the Calvin cycle to assist in the synthesis of carbohydrates from carbon dioxide and NADPH.

<span class="mw-page-title-main">Phycobilisome</span> Light-energy harvesting structure in cyanobacteria and red algae

Phycobilisomes are light harvesting antennae of photosystem II in cyanobacteria, red algae and glaucophytes. It was lost in the plastids of green algae / plants (chloroplasts).

<span class="mw-page-title-main">Light-harvesting complexes of green plants</span>

The light-harvesting complex is an array of protein and chlorophyll molecules embedded in the thylakoid membrane of plants and cyanobacteria, which transfer light energy to one chlorophyll a molecule at the reaction center of a photosystem.

<span class="mw-page-title-main">Photosynthetic reaction centre</span>

A photosynthetic reaction center is a complex of several proteins, pigments and other co-factors that together execute the primary energy conversion reactions of photosynthesis. Molecular excitations, either originating directly from sunlight or transferred as excitation energy via light-harvesting antenna systems, give rise to electron transfer reactions along the path of a series of protein-bound co-factors. These co-factors are light-absorbing molecules (also named chromophores or pigments) such as chlorophyll and pheophytin, as well as quinones. The energy of the photon is used to excite an electron of a pigment. The free energy created is then used, via a chain of nearby electron acceptors, for a transfer of hydrogen atoms (as protons and electrons) from H2O or hydrogen sulfide towards carbon dioxide, eventually producing glucose. These electron transfer steps ultimately result in the conversion of the energy of photons to chemical energy.

<span class="mw-page-title-main">Photoinhibition</span>

Photoinhibition is light-induced reduction in the photosynthetic capacity of a plant, alga, or cyanobacterium. Photosystem II (PSII) is more sensitive to light than the rest of the photosynthetic machinery, and most researchers define the term as light-induced damage to PSII. In living organisms, photoinhibited PSII centres are continuously repaired via degradation and synthesis of the D1 protein of the photosynthetic reaction center of PSII. Photoinhibition is also used in a wider sense, as dynamic photoinhibition, to describe all reactions that decrease the efficiency of photosynthesis when plants are exposed to light.

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Non-photochemical quenching (NPQ) is a mechanism employed by plants and algae to protect themselves from the adverse effects of high light intensity. It involves the quenching of singlet excited state chlorophylls (Chl) via enhanced internal conversion to the ground state, thus harmlessly dissipating excess excitation energy as heat through molecular vibrations. NPQ occurs in almost all photosynthetic eukaryotes, and helps to regulate and protect photosynthesis in environments where light energy absorption exceeds the capacity for light utilization in photosynthesis.

<span class="mw-page-title-main">Light-dependent reactions</span> Photosynthetic reactions

Light-dependent reactions is jargon for certain photochemical reactions that are involved in photosynthesis, the main process by which plants acquire energy. There are two light dependent reactions, the first occurs at photosystem II (PSII) and the second occurs at photosystem I (PSI),

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Quantasomes are particles found in the thylakoid membrane of chloroplasts in which photosynthesis takes place. They are embedded in a paracrystalline array on the surface of thylakoid discs in chloroplasts. They are composed of lipids and proteins that include various photosynthetic pigments and redox carriers. For this reason they are considered to be photosynthetic units. They occur in 2 sizes: the smaller quantasome is thought to represent the site of photosystem I, the larger to represent the site of photosystem II.

References

  1. ↑ Nixon, P. (2000). "Chlororespiration". Philosophical Transactions of the Royal Society B: Biological Sciences. 355 (1402): 355(1402), 1541–1547. doi:10.1098/rstb.2000.0714. PMC   1692878 . PMID   11128007.
  2. 1 2 3 4 5 6 7 8 9 10 11 Cournac, L.; Peltier, G. (2002). "Chlororespiration". Annual Review of Plant Biology. 53: 523–550. doi:10.1146/annurev.arplant.53.100301.135242. PMID   12227339.
  3. 1 2 3 4 5 6 7 8 9 10 11 12 Paredes, Miriam; Quiles, María José (January 2013). "Stimulation of chlororespiration by drought under heat and high illumination in Rosa meillandina". Journal of Plant Physiology. 170 (2): 165–171. doi:10.1016/j.jplph.2012.09.010. PMID   23122789.
  4. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 Quiles, M. (2006). "Stimulation of chlororespiration by heat and high light intensity in oat plants". Plant, Cell & Environment. 29 (8): 1463–1470. doi: 10.1111/j.1365-3040.2006.01510.x . PMID   16898010.
  5. 1 2 Houille-Vernes, L.; Rappaport, F.; Wollman, F.-A.; Alric, J.; Johnson, X. (2011). "Plastid terminal oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas". Proceedings of the National Academy of Sciences of the United States of America. 108 (51): 20820–20825. Bibcode:2011PNAS..10820820H. doi: 10.1073/pnas.1110518109 . PMC   3251066 . PMID   22143777.
  6. 1 2 3 4 5 Peltier, G.; Schmidt, G. W. (1991). "Chlororespiration: an adaptation to nitrogen deficiency in Chlamydomonas reinhardtii". Proceedings of the National Academy of Sciences of the United States of America. 88 (11): 4791–4795. Bibcode:1991PNAS...88.4791P. doi: 10.1073/pnas.88.11.4791 . PMC   51752 . PMID   11607187.
  7. ↑ Bennoun, P. (1982). "Evidence for a respiratory chain in the chloroplast". Proceedings of the National Academy of Sciences of the United States of America. 79 (14): 4352–4356. Bibcode:1982PNAS...79.4352B. doi: 10.1073/pnas.79.14.4352 . PMC   346669 . PMID   16593210.
  8. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Gasulla, Francisco; Casano, Leonardo; Guéra, Alfredo (2018). "Chlororespiration induces non-photochemical quenching of chlorophyll fluorescence during darkness in lichen chlorobionts". Physiologia Plantarum. 166 (2): 538–552. doi:10.1111/ppl.12792. PMID   29952012. S2CID   49473988.
  9. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 Segura, María V.; Quiles, María J. (March 2015). "Involvement of chlororespiration in chilling stress in the tropical species". Plant, Cell & Environment. 38 (3): 525–533. doi: 10.1111/pce.12406 . PMID   25041194.
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