Arbuscular Mycorrhizal Symbiosis Enhances Photosynthesis in the Medicinal Herb Salvia fruticosa by Improving Photosystem II Photochemistry
Abstract
:1. Introduction
2. Results
2.1. Mycorrhizal Colonization and Plant Growth Performance
2.2. The Allocation of Absorbed Light Energy in Inoculated and Non-inoculated Salvia
2.3. The Efficiency of PSII in Inoculated and Non-Inoculated Salvia
2.4. Chlorophyll a Fluorescence Images
3. Discussion
4. Materials and Methods
4.1. Plant Material and Growth Conditions
4.2. Arbuscular Mycorrhizal Application
4.3. Growth Measurements and Mycorrhizal Colonization Evaluation
4.4. Chlorophyll Fluorescence Imaging Analysis
4.5. Statistical Analysis
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Parniske, M. Arbuscular mycorrhiza: The mother of plant root endosymbioses. Nat. Rev. Microbiol. 2008, 6, 763. [Google Scholar] [CrossRef] [PubMed]
- Douds, D.D.; Nagahashi, G.; Reider, C.; Hepperly, P.R. Inoculation with arbuscular mycorrhizal fungi increases the yield of potatoes in a high P soil. Biol. Agric. Hortic. 2007, 25, 67–78. [Google Scholar] [CrossRef]
- Golubkina, N.; Krivenkov, L.; Sekara, A.; Vasileva, V.; Tallarita, A.; Caruso, G. Prospects of arbuscular mycorrhizal fungi utilization in production of Allium plants. Plants 2020, 9, 279. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, L.; Xu, M.; Liu, Y.; Zhang, F.; Hodge, A.; Feng, G. Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate-solubilizing bacterium. New Phytol. 2016, 210, 1022–1032. [Google Scholar] [CrossRef] [Green Version]
- Zhang, X.; Zhang, H.; Zhang, Y.; Liu, Y.; Zhang, H.; Tang, M. Arbuscular mycorrhizal fungi alter carbohydrate distribution and amino acid accumulation in Medicago truncatula under lead stress. Environ. Exp. Bot. 2020, 171, 103950. [Google Scholar] [CrossRef]
- Sheng, M.; Tang, M.; Chen, H.; Yang, B.; Zhang, F.; Huang, Y. Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 2008, 18, 287–296. [Google Scholar] [CrossRef]
- Dodd, I.C.; Ruíz-Lozano, J.M. Microbial enhancement of crop resource use efficiency. Curr. Opin. Biotechnol. 2012, 23, 236–242. [Google Scholar] [CrossRef]
- Gianinazzi, S.; Gollotte, A.; Binet, M.N.; van Tuinen, D.; Redecker, D.; Wipf, D. Agroecology: The key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 2010, 20, 519–530. [Google Scholar] [CrossRef]
- Ruiz-Sánchez, M.; Aroca, R.; Muñoz, Y.; Polón, R.; Ruiz-Lozano, J.M. The arbuscular mycorrhizal symbiosis enhances the photosynthetic Mycorrhiza efficiency and the antioxidative response of rice plants subjected to drought stress. J. Plant Physiol. 2010, 167, 862–869. [Google Scholar] [CrossRef]
- Dhawi, F.; Datta, R.; Ramakrishna, W. Mycorrhiza and heavy metal resistant bacteria enhance growth, nutrient uptake and alter metabolic profile of sorghum grown in marginal soil. Chemosphere 2016, 157, 33–41. [Google Scholar] [CrossRef]
- Zhan, F.; Li, B.; Jiang, M.; Yue, X.; He, Y.; Xia, Y.; Wang, Y. Arbuscular mycorrhizal fungi enhance antioxidant defense in the leaves and the retention of heavy metals in the roots of maize. Environ. Sci. Pollut. Res. 2018, 25, 24338–24347. [Google Scholar] [CrossRef] [PubMed]
- Begum, N.; Ahanger, M.A.; Su, Y.; Lei, Y.; Mustafa, N.S.A.; Ahmad, P.; Zhang, L. Improved drought tolerance by AMF inoculation in maize (Zea mays) involves physiological and biochemical implications. Plants 2019, 8, 579. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Boutasknit, A.; Baslam, M.; Ait-El-Mokhtar, M.; Anli, M.; Ben-Laouane, R.; Douira, A.; El Modafar, C.; Mitsui, T.; Wahbi, S.; Meddich, A. Arbuscular mycorrhizal fungi mediate drought tolerance and recovery in two contrasting carob (Ceratonia siliqua L.) ecotypes by regulating stomatal, water relations, and (in)organic adjustments. Plants 2020, 9, 80. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Singh, N.V.; Singh, S.K.; Singh, A.K.; Meshram, D.T.; Suroshe, S.S.; Mishra, D.C. Arbuscular mycorrhizal fungi (AMF) induced hardening of micropropagated pomegranate (Punica granatum L.) plantlets. Sci. Hortic. 2012, 136, 122–127. [Google Scholar] [CrossRef]
- Romero-Munar, A.; Tauler, M.; Gulías, J.; Baraza, E. Nursery preconditioning of Arundo donax L. plantlets determines biomass harvest in the first two years. Ind. Crops Prod. 2018, 119, 33–40. [Google Scholar] [CrossRef]
- Schwarzott, D.; Walker, C.; Schüssler, A. Glomus, the largest genus of the arbuscular mycorrhizal fungi (Glomales), is nonmonophyletic. Mol. Phylogenet. Evol. 2001, 21, 190–197. [Google Scholar] [CrossRef]
- Krüger, M.; Krüger, C.; Walker, C.; Stockinger, H.; Schüßler, A. Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol. 2011, 193, 970–984. [Google Scholar] [CrossRef]
- Blaszkowski, J.; Czerniawska, B.; Wubet, T.; Schuessler, T.; Buscot, F.; Renker, C. Glomus irregulare, a new arbuscular mycorrhizal fungus in the Glomeromycota. Mycotaxon 2008, 106, 247–267. [Google Scholar]
- Stockinger, H.; Walker, C.; Schüssler, A. ‘Glomus intraradices DAOM197198’, a model fungus in arbuscular mycorrhiza research, is not Glomus intraradices. New Phytol. 2009, 183, 1176–1187. [Google Scholar] [CrossRef]
- Formey, D.; Molès, M.; Haouy, A.; Savelli, B.; Bouchez, O.; Bécard, G.; Roux, C. Comparative analysis of mitochondrial genomes of Rhizophagus irregularis—syn. Glomus irregular—Reveals a polymorphism induced by variability generating elements. New Phytol. 2012, 196, 1217–1227. [Google Scholar]
- He, F.; Sheng, M.; Tang, M. Effects of Rhizophagus irregularis on photosynthesis and antioxidative enzymatic system in Robinia pseudoacacia L. under drought stress. Front. Plant Sci. 2017, 8, 183. [Google Scholar] [CrossRef] [Green Version]
- Le Pioufle, O.; Ganoudi, M.; Calonne-Salmon, M.; Dhaou, F.B.; Declerck, S. Rhizophagus irregularis MUCL 41833 improves phosphorus uptake and water use efficiency in maize plants during recovery from drought stress. Front. Plant Sci. 2019, 10, 897. [Google Scholar] [CrossRef] [Green Version]
- Golubkina, N.; Logvinenko, L.; Novitsky, M.; Zamana, S.; Sokolov, S.; Molchanova, A.; Shevchuk, O.; Sekara, A.; Tallarita, A.; Caruso, G. Yield, essential oil and quality performances of Artemisia dracunculus, Hyssopus officinalis and Lavandula angustifolia as affected by arbuscular mycorrhizal fungi under organic management. Plants 2020, 9, 375. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kushwaha, R.K.; Rodrigues, V.; Kumar, V.; Patel, H.; Raina, M.; Kumar, D. Soil microbes-medicinal plants interactions: Ecological diversity and future prospect. In Plant Microbe Symbiosis; Varma, A., Tripathi, S., Prasad, R., Eds.; Springer: Cham, Switzerland, 2020; pp. 263–286. [Google Scholar]
- Zubek, S.; Błaszkowski, J. Medicinal plants as hosts of arbuscular mycorrhizal fungi and dark septate endophytes. Phytochem. Rev. 2009, 8, 571–580. [Google Scholar] [CrossRef]
- Moustaka, J.; Ouzounidou, G.; Sperdouli, I.; Moustakas, M. Photosystem II is more sensitive than photosystem I to Al3+ induced phytotoxicity. Materials 2018, 11, 1772. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sperdouli, I.; Moustaka, J.; Antonoglou, O.; Adamakis, I.D.S.; Dendrinou-Samara, C.; Moustakas, M. Leaf age dependent effects of foliar-sprayed CuZn nanoparticles on photosynthetic efficiency and ROS generation in Arabidopsis thaliana. Materials 2019, 12, 2498. [Google Scholar] [CrossRef] [Green Version]
- Flood, P.J.; Harbinson, J.; Aarts, M.G. Natural genetic variation in plant photosynthesis. Trends Plant Sci. 2011, 16, 327–335. [Google Scholar] [CrossRef]
- Anderson, J.M. Changing concepts about the distribution of photosystems I and II between grana-appressed and stroma-exposed thylakoid membranes. Photosynth. Res. 2002, 73, 157–164. [Google Scholar] [CrossRef]
- Antonoglou, O.; Moustaka, J.; Adamakis, I.D.; Sperdouli, I.; Pantazaki, A.; Moustakas, M.; Dendrinou-Samara, C. Nanobrass CuZn nanoparticles as foliar spray non phytotoxic fungicides. ACS Appl. Mater. Interfaces 2018, 10, 4450–4461. [Google Scholar] [CrossRef]
- Krause, G.; Weis, E. Chlorophyll fluorescence and photosynthesis: The basics. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1991, 42, 313–349. [Google Scholar] [CrossRef]
- Asfi, M.; Ouzounidou, G.; Panajiotidis, S.; Therios, I.; Moustakas, M. Toxicity effects of olive-mill wastewater on growth, photosynthesis and pollen morphology of spinach plants. Ecotoxicol. Environ. Saf. 2012, 80, 69–75. [Google Scholar] [CrossRef] [PubMed]
- Asfi, M.; Ouzounidou, G.; Moustakas, M. Evaluation of olive oil mill wastewater toxicity on spinach. Environ. Sci. Pollut. Res. 2012, 19, 2363–2371. [Google Scholar] [CrossRef] [PubMed]
- Murchie, E.H.; Lawson, T. Chlorophyll fluorescence analysis: A guide to good practice and understanding some new applications. J. Exp. Bot. 2013, 64, 3983–3998. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sperdouli, I.; Moustakas, M. Differential blockage of photosynthetic electron flow in young and mature leaves of Arabidopsis thaliana by exogenous proline. Photosynthetica 2015, 53, 471–477. [Google Scholar] [CrossRef]
- Kalaji, H.M.; Jajoo, A.; Oukarroum, A.; Brestic, M.; Zivcak, M.; Samborska, I.A.; Cetner, M.D.; Łukasik, I.; Goltsev, V.; Ladle, R.J. Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol. Plant. 2016, 38, 1–11. [Google Scholar] [CrossRef] [Green Version]
- Moustaka, J.; Ouzounidou, G.; Bayçu, G.; Moustakas, M. Aluminum resistance in wheat involves maintenance of leaf Ca2+ and Mg2+ content, decreased lipid peroxidation and Al accumulation, and low photosystem II excitation pressure. BioMetals 2016, 29, 611–623. [Google Scholar] [CrossRef]
- Kalaji, H.M.; Račková, L.; Paganová, V.; Swoczyna, T.; Rusinowski, S.; Sitko, K. Can chlorophyll-a fluorescence parameters be used as bio-indicators to distinguish between drought and salinity stress in Tilia cordata Mill? Environ. Exp. Bot. 2018, 152, 149–157. [Google Scholar] [CrossRef]
- Barbagallo, R.P.; Oxborough, K.; Pallett, K.E.; Baker, N.R. Rapid, noninvasive screening for perturbations of metabolism and plant growth using chlorophyll fluorescence imaging. Plant Physiol. 2003, 132, 485–493. [Google Scholar] [CrossRef] [Green Version]
- Gorbe, E.; Calatayud, A. Applications of chlorophyll fluorescence imaging technique in horticultural research: A review. Sci. Hortic. 2012, 138, 24–35. [Google Scholar] [CrossRef]
- Chaerle, L.; Lenk, S.; Hagenbeek, D.; Buschmann, C.; Van Der Straeten, D. Multi-color fluorescence imaging for early detection of the hypersensitive reaction to tobacco mosaic virus. J. Plant Physiol. 2007, 164, 253–262. [Google Scholar] [CrossRef]
- Sperdouli, I.; Moustakas, M. Spatio-temporal heterogeneity in Arabidopsis thaliana leaves under drought stress. Plant Biol. 2012, 14, 118–128. [Google Scholar] [CrossRef] [PubMed]
- Martinez-Penalver, A.; Reigosa, M.J.; Sanchez-Moreiras, A.M. Imaging chlorophyll a fluorescence reveals specific spatial distributions under different stress conditions. Flora 2011, 206, 836–844. [Google Scholar] [CrossRef]
- Moustakas, M.; Malea, P.; Zafeirakoglou, A.; Sperdouli, I. Photochemical changes and oxidative damage in the aquatic macrophyte Cymodocea nodosa exposed to paraquat-induced oxidative stress. Pest. Biochem. Physiol. 2016, 126, 28–34. [Google Scholar] [CrossRef] [PubMed]
- Bayçu, G.; Moustaka, J.; Gevrek-Kürüm, N.; Moustakas, M. Chlorophyll fluorescence imaging analysis for elucidating the mechanism of photosystem II acclimation to cadmium exposure in the hyperaccumulating plant Noccaea caerulescens. Materials 2018, 11, 2580. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moustakas, M.; Hanć, A.; Dobrikova, A.; Sperdouli, I.; Adamakis, I.D.S.; Apostolova, E. Spatial heterogeneity of cadmium effects on Salvia sclarea leaves revealed by chlorophyll fluorescence imaging analysis and laser ablation inductively coupled plasma mass spectrometry. Materials 2019, 12, 2953. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moustakas, M.; Bayçu, G.; Gevrek-Kürüm, N.; Moustaka, J.; Csatári, I.; Rognes, S.E. Spatiotemporal heterogeneity of photosystem II function during acclimation to zinc exposure and mineral nutrition changes in the hyperaccumulator Noccaea caerulescens. Environ. Sci. Pollut. Res. 2019, 26, 6613–6624. [Google Scholar] [CrossRef]
- Kramer, D.M.; Johnson, G.; Kiirats, O.; Edwards, G.E. New fluorescence parameters for determination of QA redox state and excitation energy fluxes. Photosynth. Res. 2004, 79, 209–218. [Google Scholar] [CrossRef]
- Gutierrez-Manero, F.J.; Ramos-Solano, B.; Probanza, A.; Mehouachi, J.; Tadeo, F.R.; Talon, M. The plant-growth-promoting rhizobacteriaBacillus pumilusandBacillus licheniformisproduce high amounts of physiologically active gibberellins. Physiol. Plant. 2001, 111, 206–211. [Google Scholar] [CrossRef]
- Ramírez-Flores, M.R.; Bello-Bello, E.; Rellán-Álvarez, R.; Sawers, R.J.H.; Olalde-Portuga, V. Inoculation with the mycorrhizal fungus Rhizophagus irregularis modulates the relationship between root growth and nutrient content in maize (Zea mays ssp. mays L.). Plant Direct. 2019, 3, 1–12. [Google Scholar]
- Li, N.; Chen, Y.R.; Ding, Z.; Li, P.; Wu, Y.; Zhang, A.; Yu, S.; Giovannoni, J.J.; Fei, Z.; Zhang, W.; et al. Nonuniform gene expression pattern detected along the longitudinal axis in the matured rice leaf. Sci. Rep. 2015, 5, 8015. [Google Scholar] [CrossRef] [Green Version]
- Jiang, C.D.; Li, P.M.; Gao, H.Y.; Zou, Q.; Jiang, G.M.; Li, L.H. Enhanced photoprotection at the early stages of leaf expansion in field-grown soybean plants. Plant Sci. 2005, 168, 911–919. [Google Scholar] [CrossRef]
- Sperdouli, I.; Moustakas, M. Differential response of photosystem II photochemistry in young and mature leaves of Arabidopsis thaliana to the onset of drought stress. Acta Physiol. Plant. 2012, 34, 1267–1276. [Google Scholar] [CrossRef]
- Sperdouli, I.; Moustakas, M. A better energy allocation of absorbed light in photosystem II and less photooxidative damage contribute to acclimation of Arabidopsis thaliana young leaves to water deficit. J. Plant Physiol. 2014, 171, 587–593. [Google Scholar] [CrossRef] [PubMed]
- Sperdouli, I.; Moustakas, M. Leaf developmental stage modulates metabolite accumulation and photosynthesis contributing to acclimation of Arabidopsis thaliana to water deficit. J. Plant Res. 2014, 127, 481–489. [Google Scholar] [CrossRef]
- Moustaka, J.; Tanou, G.; Adamakis, I.D.; Eleftheriou, E.P.; Moustakas, M. Leaf age dependent photoprotective and antioxidative mechanisms to paraquat-induced oxidative stress in Arabidopsis thaliana. Int. J. Mol. Sci. 2015, 16, 13989–14006. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bielczynski, L.W.; Łącki, M.K.; Hoefnagels, I.; Gambin, A.; Croce, R. Leaf and plant age affects photosynthetic performance and photoprotective capacity. Plant Physiol. 2017, 175, 1634–1648. [Google Scholar] [CrossRef] [PubMed]
- Müller, P.; Li, X.P.; Niyogi, K.K. Non-photochemical quenching. A response to excess light energy. Plant Physiol. 2001, 125, 1558–1566. [Google Scholar] [CrossRef] [Green Version]
- Kasajima, I.; Ebana, K.; Yamamoto, T.; Takahara, K.; Yano, M.; Kawai-Yamada, M.; Uchimiya, H. Molecular distinction in genetic regulation of nonphotochemical quenching in rice. Proc. Natl. Acad. Sci. USA 2011, 108, 13835–13840. [Google Scholar] [CrossRef] [Green Version]
- Gawroński, P.; Witoń, D.; Vashutina, K.; Bederska, M.; Betliński, B.; Rusaczonek, A.; Karpiński, S. Mitogen-activated protein kinase 4 is a salicylic acid-independent regulator of growth but not of photosynthesis in Arabidopsis. Mol. Plant 2014, 7, 1151–1166. [Google Scholar] [CrossRef] [Green Version]
- Moustaka, J.; Tanou, G.; Giannakoula, A.; Panteris, E.; Eleftheriou, E.P.; Moustakas, M. Anthocyanin accumulation in poinsettia leaves and its functional role in photo-oxidative stress. Environ. Exp. Bot. 2020, 175, 104065. [Google Scholar] [CrossRef]
- Hideg, É.; Spetea, C.; Vass, I. Singlet oxygen production in thylakoid membranes during photoinhibition as detected by EPR spectroscopy. Photosynth. Res. 1994, 39, 191–199. [Google Scholar] [CrossRef] [PubMed]
- op den Camp, R.G.L.; Przybyla, D.; Ochsenbein, C.; Laloi, C.; Kim, C.; Danon, A.; Wagner, D.; Hideg, É.; Göbel, C.; Feussner, I.; et al. Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 2003, 15, 2320–2332. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Krieger-Liszkay, A.; Fufezan, C.; Trebst, A. Singlet oxygen production in photosystem II and related protection mechanism. Photosynth. Res. 2008, 98, 551–564. [Google Scholar] [CrossRef]
- Triantaphylidès, C.; Havaux, M. Singlet oxygen in plants: Production, detoxification and signaling. Trends Plant Sci. 2009, 14, 219–228. [Google Scholar] [CrossRef]
- Telfer, A. Singlet oxygen production by PSII under light stress: Mechanism, detection and the protective role of beta-carotene. Plant Cell Physiol. 2014, 55, 1216–1223. [Google Scholar] [CrossRef] [Green Version]
- Roach, T.; Na, C.S.; Stöggl, W.; Krieger-Liszkay, A. The non-photochemical quenching protein LHCSR3 prevents oxygen-dependent photoinhibition in Chlamydomonas reinhardtii. J. Exp. Bot. 2020, 71, 2650–2660. [Google Scholar] [CrossRef]
- Genty, B.; Briantais, J.M.; Baker, N.R. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta 1989, 990, 87–92. [Google Scholar] [CrossRef]
- Simón, I.; Díaz-López, L.; Gimeno, V.; Nieves, M.; Pereira, W.E.; Martínez, V.; Lidon, V.; García-Sánchez, F. Effects of boron excess in nutrient solution on growth, mineral nutrition, and physiological parameters of Jatropha curcas seedlings. J. Plant Nutr. Soil Sci. 2013, 176, 165–174. [Google Scholar] [CrossRef]
- Demmig-Adams, B.; Cohu, C.M.; Muller, O.; Adams, W.W. Modulation of photosynthetic energy conversion efficiency in nature: From seconds to seasons. Photosynth. Res. 2012, 113, 75–88. [Google Scholar] [CrossRef]
- Takahashi, S.; Badger, M.R. Photoprotection in plants: A new light on photosystem II damage. Trends Plant Sci. 2011, 16, 53–60. [Google Scholar] [CrossRef]
- Moustaka, J.; Moustakas, M. Photoprotective mechanism of the non-target organism Arabidopsis thaliana to paraquat exposure. Pest. Biochem. Physiol. 2014, 111, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Ruban, A.V. Nonphotochemical chlorophyll fluorescence quenching: Mechanism and effectiveness in protecting plants from photodamage. Plant Physiol. 2016, 170, 1903–1916. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nishiyama, Y.; Yamamoto, H.; Allakhverdiev, S.I.; Inaba, M.; Yokota, A.; Murata, N. Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J. 2001, 20, 5587–5594. [Google Scholar] [CrossRef] [PubMed]
- Murata, N.; Takahashi, S.; Nishiyama, Y.; Allakhverdiev, S.I. Photoinhibition of photosystem II under environmental stress. Biochim. Biophys. Acta 2007, 1767, 414–421. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Roach, T.; Sedoud, A.; Krieger-Liszkay, A. Acetate in mixotrophic growth medium affects photosystem II in Chlamydomonas reinhardtii and protects against photoinhibition. Biochim. Biophys. Acta 2013, 1827, 1183–1190. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kale, R.; Hebert, A.E.; Frankel, L.K.; Sallans, L.; Bricker, T.M.; Pospíšil, P. Amino acid oxidation of the D1 and D2 proteins by oxygen radicals during photoinhibition of Photosystem II. Proc. Natl. Acad. Sci. USA 2017, 114, 2988–2993. [Google Scholar] [CrossRef] [Green Version]
- Bilger, W.; Schreiber, U.; Bock, M. Determination of the quantum efficiency of photosystem II and of non-photochemical quenching of chlorophyll fluorescence in the field. Oecologia 1995, 102, 425–432. [Google Scholar] [CrossRef]
- Lima, C.S.; Ferreira-Silva, S.L.; Carvalho, F.E.L.; Neto, M.C.L.; Aragăo, R.M.; Silva, E.N.; Sousa, R.M.J.; Silveira, J.A.G. Antioxidant protection and PSII regulation mitigate photo-oxidative stress induced by drought followed by high light in cashew plants. Environ. Exp. Bot. 2018, 149, 59–69. [Google Scholar] [CrossRef] [Green Version]
- Li, X.P.; Muller-Moule, P.; Gilmore, A.M.; Niyogi, K.K. PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc. Natl Acad. Sci. USA 2002, 99, 15222–15227. [Google Scholar] [CrossRef] [Green Version]
- Krah, N.; Logan, B.A. Loss of psbS expression reduces vegetative growth, reproductive output, and light-limited, but not light-saturated, photosynthesis in Arabidopsis thaliana (Brassicaceae) grown in temperate light environments. Am. J. Bot. 2010, 97, 644–649. [Google Scholar] [CrossRef]
- Hubbart, S.; Smillie, I.; Heatley, M.; Swarup, R.; Foo, C.; Zhao, L.; Murchie, E. Enhanced thylakoid photoprotection can increase yield and canopy radiation use efficiency in rice. Commun. Biol. 2018, 1, 22. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ruban, A.V. Evolution under the sun: Optimizing light harvesting in photosynthesis. J. Exp. Bot. 2015, 66, 7–23. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Murchie, E.H.; Ruban, A.V. Dynamic non-photochemical quenching in plants: From molecular mechanism to productivity. Plant J. 2020, 101, 885–896. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Busch, F.A. Opinion: The red-light response of stomatal movement is sensed by the redox state of the photosynthetic electron transport chain. Photosynth. Res. 2014, 119, 131–140. [Google Scholar] [CrossRef] [PubMed]
- Glowacka, K.; Kromdijk, J.; Kucera, K.; Xie, J.; Cavanagh, A.P.; Leonelli, L.; Leakey, A.D.B.; Ort, D.R.; Niyogi, K.K.; Long, S.P. Photosystem II Subunit S over-expression increases the efficiency of water use in a field-grown crop. Nat. Commun. 2018, 9, 868. [Google Scholar] [CrossRef] [Green Version]
- Kromdijk, J.; Głowacka, K.; Long, S.P. Predicting light-induced stomatal movements based on the redox state of plastoquinone: Theory and validation. Photosynth. Res. 2019, 141, 83–97. [Google Scholar] [CrossRef] [Green Version]
- Kaiser, E.; Correa Galvis, V.; Armbruster, U. Efficient photosynthesis in dynamic light environments: A chloroplast’s perspective. Biochem. J. 2019, 476, 2725–2741. [Google Scholar] [CrossRef] [Green Version]
- McAusland, L.; Davey, P.; Kanwal, N.; Baker, N.; Lawson, T.A. Novel system for spatial and temporal imaging of intrinsic plant water use efficiency. J. Exp. Bot. 2013, 64, 4993–5007. [Google Scholar] [CrossRef] [Green Version]
- Kitajima, H.; Butler, W.L. Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymo-quinone. Biochim. Biophys. Acta 1975, 376, 105–115. [Google Scholar] [CrossRef]
- Babani, F.; Lichtenthaler, H.K. Light-induced and age-dependent development of chloroplasts in etiolated barley leaves as visualized by determination of photosynthetic pigments, CO2 assimilation rates and different kinds of chlorophyll fluorescence ratios. J. Plant Physiol. 1996, 148, 555–566. [Google Scholar] [CrossRef]
- Lichtenthaler, H.K.; Babani, F.; Langsdorf, G. Chlorophyll fluorescence imaging of photosynthetic activity in sun and shade leaves of trees. Photosynth Res. 2007, 93, 235–244. [Google Scholar] [CrossRef] [PubMed]
- Pereira, W.E.; De Siqueira, D.L.; Martinez, C.A.; Puiatti, M. Gas exchange and chlorophyll fluorescence in four citrus rootstocks under aluminium stress. J. Plant Physiol. 2000, 157, 513–520. [Google Scholar] [CrossRef]
- Pellegrini, E.; Carucci, M.G.; Campanella, A.; Lorenzini, G.; Nali, C. Ozone stress in Melissa officinalis plants assessed by photosynthetic function. Environ. Exp. Bot. 2011, 73, 94–101. [Google Scholar] [CrossRef]
- Govindachary, S.; Bukhov, N.G.; Joly, D.; Carpentier, R. Photosystem II inhibition by moderate light under low temperature in intact leaves of chilling-sensitive and -tolerant plants. Physiol. Plant. 2004, 121, 322–333. [Google Scholar] [CrossRef]
- Mosadegh, H.; Trivellini, A.; Lucchesini, M.; Ferrante, A.; Maggini, R.; Vernieri, P.; Mensuali Sodi, A. UV-B physiological changes under conditions of distress and eustress in sweet basil. Plants 2019, 8, 396. [Google Scholar] [CrossRef] [Green Version]
- Callahan, F.E.; Becker, D.W.; Cheniae, G.M. Studies on the photo-inactivation of the water-oxidizing enzyme. II. Characterization of weak light photoinhibition of PSII and its light-induced recovery. Plant Physiol. 1986, 82, 261–269. [Google Scholar] [CrossRef] [Green Version]
- Chen, G.X.; Kazimir, J.; Cheniae, G.M. Photoinhibition of hydroxylamine-extracted photosystem II membranes: Studies of the mechanism. Biochemistry 1992, 31, 11072–11083. [Google Scholar] [CrossRef]
- Anderson, J.M.; Park, Y.I.; Chow, W.S. Unifying model for the photoinactivation of photosystem II in vivo: A hypothesis. Photosynth. Res. 1998, 56, 1–13. [Google Scholar] [CrossRef]
- Sarvikas, P.; Hakala, M.; Pätsikkä, E.; Tyystjärvi, T.; Tyystjärvi, E. Action spectrum of photoinhibition in leaves of wild type and npq1-2 and npq4-1 mutants of Arabidopsis thaliana. Plant Cell Physiol. 2006, 47, 391–400. [Google Scholar] [CrossRef] [Green Version]
- Demmig, B.; Björkman, O. Comparison of the effect of excessive light on chlorophyll fluorescence (77K) and photon yield of O2 evolution in leaves of higher plants. Planta 1987, 171, 171–184. [Google Scholar] [CrossRef]
- Franklin, L.A.; Levavasseur, G.; Osmond, C.B.; Henley, W.J.; Ramus, J. Two components of onset and recovery during photoinhibition of Ulva rotundata. Planta 1992, 186, 399–408. [Google Scholar] [CrossRef] [PubMed]
- Osmond, B. What is photoinhibition? Some insights from comparisons of shade and sun plants. In Photoinhibition of Photosynthesis from Molecular Mechanisms to the Field; Baker, N.R., Bowyer, J.R., Eds.; Bios Scientific Publishing Ltd.: Oxford, UK, 1994; pp. 1–24. [Google Scholar]
- Park, Y.I.; Chow, W.S.; Anderson, J.M. Light inactivation of functional photosystem-II in leaves of peas grown in moderate light depends on photon exposure. Planta 1995, 196, 401–411. [Google Scholar] [CrossRef]
- Oguchi, R.; Terashima, I.; Chow, W.S. The involvement of dual mechanisms of photoinactivation of photosystem II in Capsicum annuum L. plants. Plant Cell Physiol. 2009, 50, 1815–1825. [Google Scholar] [CrossRef] [PubMed]
- Wilson, S.; Ruban, A.V. Quantitative assessment of the high-light tolerance in plants with an impaired photosystem II donor side. Biochem. J. 2019, 476, 1377–1386. [Google Scholar] [CrossRef]
- Zhang, C.; Wang, H.; Xu, Y.; Zhang, S.; Wang, J.; Hu, B.; Hou, X.; Li, Y.; Liu, T. Enhanced relative electron transport rate contributes to increased photosynthetic capacity in autotetraploid pak choi. Plant Cell Physiol. 2020, 61, 761–774. [Google Scholar] [CrossRef]
- Romero-Munar, A.; Fernández Del-Saz, N.; Ribas-Carbó, M.; Flexas, J.; Baraza, E.; Florez-Sarasa, I.; Fernie, A.R.; Gulías, J. Arbuscular mycorrhizal symbiosis with Arundo donax decreases root respiration and increases both photosynthesis and plant biomass accumulation. Plant Cell Environ. 2017, 40, 1115–1126. [Google Scholar] [CrossRef]
- Bayçu, G.; Gevrek-Kürüm, N.; Moustaka, J.; Csatári, I.; Rognes, S.E.; Moustakas, M. Cadmium-zinc accumulation and photosystem II responses of Noccaea caerulescens to Cd and Zn exposure. Environ. Sci. Pollut. Res. 2017, 24, 2840–2850. [Google Scholar] [CrossRef]
- Höpfner, I. Competition and facilitation among grassland plants—The role of arbuscular mycorrhiza. Ph.D. Thesis, Faculty of Biology, University of Bielefeld, Bielefeld, Germany, December 2014. [Google Scholar]
- Giovannetti, M.; Mosse, B. An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol. 1980, 84, 489–500. [Google Scholar] [CrossRef]
- Phillips, J.M.; Hayman, D.S. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 1970, 55, 158–161. [Google Scholar] [CrossRef]
- Moustaka, J.; Panteris, E.; Adamakis, I.D.S.; Tanou, G.; Giannakoula, A.; Eleftheriou, E.P.; Moustakas, M. High anthocyanin accumulation in poinsettia leaves is accompanied by thylakoid membrane unstacking, acting as a photoprotective mechanism, to prevent ROS formation. Environ. Exp. Bot. 2018, 154, 44–55. [Google Scholar] [CrossRef]
- Kalaji, M.H.; Carpentier, R.; Allakhverdiev, S.I.; Bosa, K. Fluorescence parameters as an early indicator of light stress in barley. J. Photochem. Photobiol. B. 2012, 112, 1–6. [Google Scholar] [CrossRef]
- Oxborough, K.; Baker, N.R. Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components–calculation of qP and Fv′/Fm′ without measuring Fo′. Photosynth. Res. 1997, 54, 135–142. [Google Scholar] [CrossRef]
Nutrient Elements | Stock Solution (g L-1) | Used in Nutrient Solution (ml L-1) | |
---|---|---|---|
KH2PO4 | 32.93 | 2.00 | |
K2SO4 | 29.07 | 2.00 | |
MgSO4.7H2O | 30.42 | 4.00 | |
CaCl2.2H2O | 11.00 | 4.00 | |
NH4NO3 | 56.00 | 5.00 | |
MnCl2.4H2O | 1.443 | 1.00 | |
NaMoO4.2H2O | 0.018 | 1.00 | |
H3BO3 | 0.018 | 1.00 | |
CuSO4.5H2O | 0.008 | 1.00 | |
ZnSO4.7H2O | 1.44 | 1.00 | |
FeSO4.7H2O + + Titriplex III EDTA | 7.00+9.30 | 1.00 |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Moustakas, M.; Bayçu, G.; Sperdouli, I.; Eroğlu, H.; Eleftheriou, E.P. Arbuscular Mycorrhizal Symbiosis Enhances Photosynthesis in the Medicinal Herb Salvia fruticosa by Improving Photosystem II Photochemistry. Plants 2020, 9, 962. https://doi.org/10.3390/plants9080962
Moustakas M, Bayçu G, Sperdouli I, Eroğlu H, Eleftheriou EP. Arbuscular Mycorrhizal Symbiosis Enhances Photosynthesis in the Medicinal Herb Salvia fruticosa by Improving Photosystem II Photochemistry. Plants. 2020; 9(8):962. https://doi.org/10.3390/plants9080962
Chicago/Turabian StyleMoustakas, Michael, Gülriz Bayçu, Ilektra Sperdouli, Hilal Eroğlu, and Eleftherios P. Eleftheriou. 2020. "Arbuscular Mycorrhizal Symbiosis Enhances Photosynthesis in the Medicinal Herb Salvia fruticosa by Improving Photosystem II Photochemistry" Plants 9, no. 8: 962. https://doi.org/10.3390/plants9080962