Photosynthetica 2022, 60(1):59-69 | DOI: 10.32615/ps.2021.065

Intersections: photosynthesis, abiotic stress, and the plant microbiome

B. DEMMIG-ADAMS1, S.K. POLUTCHKO1, M.C. ZENIR1, P. FOUROUNJIAN2, J.J. STEWART1, M. LÓPEZ-POZO1, W.W. ADAMS III1
1 Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309, USA
2 International Lemna Association, Denville, NJ 07834, USA

Climate change impacts environmental conditions that affect photosynthesis. This review examines the effect of combinations of elevated atmospheric CO2, long photoperiods, and/or unfavorable nitrogen supply. Under moderate stress, perturbed plant source-sink ratio and redox state can be rebalanced but may result in reduced foliar protein content in C3 plants and a higher carbon-to-nitrogen ratio of plant biomass. More severe environmental conditions can trigger pronounced photosynthetic downregulation and impair growth. We comprehensively evaluate available evidence that microbial partners may be able to support plant productivity under challenging environmental conditions by providing (1) nutrients, (2) an additional carbohydrate sink, and (3) regulators of plant metabolism, especially plant redox state. In evaluating the latter mechanism, we note parallels to metabolic control in photosymbioses and microbial regulation of human redox biology.

Additional key words: carbohydrate; electron transport; homeostasis; nitrogen; reactive oxygen species; redox signaling.

Received: September 23, 2021; Revised: September 23, 2021; Accepted: December 7, 2021; Prepublished online: January 13, 2022; Published: March 18, 2022  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
DEMMIG-ADAMS, B., POLUTCHKO, S.K., ZENIR, M.C., FOUROUNJIAN, P., STEWART, J.J., LÓPEZ-POZO, M., & ADAMS III, W.W. (2022). Intersections: photosynthesis, abiotic stress, and the plant microbiome. Photosynthetica, 60(SPECIAL ISSUE 2022), 59-69. doi: 10.32615/ps.2021.065
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Acosta K., Appenroth K.J., Borisjuk L. et al.: Return of the Lemnaceae: duckweed as a model plant system in the genomics and postgenomics era. - Plant Cell 33: 3207-3234. 2021. Go to original source...
    2. Acosta K., Xu J., Gilbert S. et al.: Duckweed hosts a taxonomically similar bacterial assemblage as the terrestrial leaf microbiome. - PLoS ONE 15: e0228560, 2020. Go to original source...
    3. Adams W.W. III, Muller O., Cohu C.M., Demmig-Adams B.: May photoinhibition be a consequence, rather than a cause, of limited plant productivity? - Photosynth. Res. 117: 31-44, 2013. Go to original source...
    4. Adams W.W. III, Muller O., Cohu C.M., Demmig-Adams B.: Photosystem II efficiency and non-photochemical quenching in the context of source-sink balance. - In: Demmig-Adams B., Garab G., Adams W.W. III, Govindjee (ed.): Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Advances in Photosynthesis and Respiration. Pp. 503-529. Springer, Dordrecht 2014. Go to original source...
    5. Adams W.W. III, Stewart J.J., Demmig-Adams B.: Photosynthetic modulation in response to plant activity and the environment. - In: Adams W.W. III, Terashima I. (ed.): The Leaf: A Platform for Performing Photosynthesis. Advances in Photosynthesis and Respiration. Pp. 493-563. Springer, Dordrecht 2018. Go to original source...
    6. Adams W.W. III, Zarter C.R., Mueh K.E. et al.: Energy dissipation and photoinhibition: a continuum of photoprotection. - In: Demmig-Adams B., Adams W.W. III, Mattoo A.K. (ed.): Photoprotection, Photoinhibition, Gene Regulation, and Environment. Advances in Photosynthesis and Respiration. Pp. 49-64. Springer, Dordrecht 2006.
    7. Adavi S.B., Sathee L.: Elevated CO2 alters tissue balance of nitrogen metabolism and downregulates nitrogen assimilation and signalling gene expression in wheat seedlings receiving high nitrate supply. - Protoplasma 258: 219-233, 2021a. Go to original source...
    8. Adavi S.B., Sathee L.: Elevated CO2 differentially regulates root nitrate transporter kinetics in a genotype and nitrate dose-dependent manner. - Plant Sci. 305: 110807, 2021b. Go to original source...
    9. Agüera E., De la Haba P.: Leaf senescence in response to elevated atmospheric CO2 concentration and low nitrogen supply. - Biol. Plantarum 62: 401-408, 2018. Go to original source...
    10. Ainsworth E.A., Long S.P.: 30 years of free-air carbon dioxide enrichment (FACE): What have we learned about future crop productivity and its potential for adaptation? - Glob. Change Biol. 27: 27-49, 2021. Go to original source...
    11. Ainsworth E.A., Rogers A., Nelson R., Long S.P.: Testing the "source-sink" hypothesis of down-regulation of photosynthesis in elevated [CO2] in the field with single gene substitutions in Glycine max. - Agr. Forest Meteorol. 122: 85-94, 2004. Go to original source...
    12. Andrade A., Wolfe D.W., Fereres E.: Leaf expansion, photosynthesis, and water relations of sunflower plants grown on compacted soil. - Plant Soil 149: 175-184, 1993. Go to original source...
    13. Aranjuelo I., Ebbets A.L., Evans R.D. et al.: Maintenance of C sinks sustains enhanced C assimilation during long-term exposure to elevated [CO2] in Mojave Desert shrubs. - Oecologia 167: 339-354, 2011. Go to original source...
    14. Aranjuelo I., Pérez P., Hernández L. et al.: The response of nodulated alfalfa to water supply, temperature and elevated CO2: photosynthetic downregulation. - Physiol. Plantarum 123: 348-358, 2005. Go to original source...
    15. Asha A.D., Nivetha N., Krishna G.K. et al.: Amelioration of short-term drought stress during different growth stages in Brassica juncea by rhizobacteria mediated maintenance of ROS homeostasis. - Physiol. Plantarum 172: 1880-1893, 2021. Go to original source...
    16. Bahrami H., De Kok L.J., Armstrong R. et al.: The proportion of nitrate in leaf nitrogen, but not changes in root growth, are associated with decreased grain protein in wheat under elevated [CO2]. - J. Plant Physiol. 216: 44-51, 2017. Go to original source...
    17. Ballard J.W.O., Towarnicki S.G.: Mitochondria, the gut microbiome and ROS. - Cell. Signal. 75: 109737, 2020. Go to original source...
    18. Becklin K.M., Mullinix G.W.R., Ward J.K.: Host plant physiology and mycorrhizal functioning shift across a glacial through future [CO2] gradient. - Plant Physiol. 172: 789-801, 2016. Go to original source...
    19. Bian Z., Wang Y., Zhang X. et al.: A review of environment effects on nitrate accumulation in leafy vegetables grown in controlled environments. - Foods 9: 732, 2020. Go to original source...
    20. Blanco N.E., Ceccoli R.D., Vía M.V.D. et al.: Expression of the minor isoform pea ferredoxin in tobacco alters photosynthetic electron partitioning and enhances cyclic electron flow. - Plant Physiol. 161: 866-879, 2013. Go to original source...
    21. Bloom A.J.: The increasing importance of distinguishing among plant nitrogen sources. - Curr. Opin. Plant Biol. 25: 10-16, 2015. Go to original source...
    22. Burnett A.C., Rogers A., Rees M., Osborne C.P.: Nutrient sink limitation constrains growth in two barley species with contrasting growth strategies. - Plant Direct 2: e00094, 2018. Go to original source...
    23. Busch F.A., Sage R.F., Farquhar G.D.: Plants increase CO2 uptake by assimilating nitrogen via the photorespiratory pathway. - Nat. Plants 4: 46-54, 2018. Go to original source...
    24. Carlson-Nilsson U., Aloisi K., Vågen I.M. et al.: Trait expression and environmental responses of pea (Pisum sativum L.) genetic resources targeting cultivation in the Arctic. - Front. Plant Sci. 12: 688067, 2021. Go to original source...
    25. Chaput V., Martin A., Lejay L., Doerner P.: Redox metabolism: The hidden player in carbon and nitrogen signaling? - J. Exp. Bot. 71: 3816-3826, 2020. Go to original source...
    26. Chen J., Zhang H., Zhang X., Tang M.: Arbuscular mycorrhizal symbiosis alleviates salt stress in black locust through improved photosynthesis, water status, and K+/Na+ homeostasis. - Front. Plant Sci. 8: 1739, 2017. Go to original source...
    27. Chouhan G.K., Verma J.P., Jaiswal D.K. et al.: Phytomicrobiome for promoting sustainable agriculture and food security: opportunities, challenges, and solutions. - Microbiol. Res. 248: 126763, 2021. Go to original source...
    28. Courteille A., Vesa S., Sanz-Barrio R. et al.: Thioredoxin m4 controls photosynthetic alternative electron pathways in Arabidopsis. - Plant Physiol. 161: 508-520, 2013. Go to original source...
    29. Dai N., Schaffer A., Petreikov M. et al.: Overexpression of Arabidopsis hexokinase in tomato plants inhibits growth, reduces photosynthesis, and induces rapid senescence. - Plant Cell 11: 1253-1266, 1999. Go to original source...
    30. de Sousa Leite T., Monteiro F.A.: Partial replacement of nitrate by ammonium increases photosynthesis and reduces oxidative stress in tanzania guinea grass exposed to cadmium. - Ecotox. Environ. Safe. 174: 592-600, 2019. Go to original source...
    31. Demmig-Adams B., Cohu C.M., Muller O., Adams W.W. III: Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons. - Photosynth. Res. 113: 75-88, 2012. Go to original source...
    32. Demmig-Adams B., Stewart J.J., Adams W.W. III: Photoprotection and the trade-off between abiotic and biotic defense. - In: Demmig-Adams B., Garab G., Adams W.W. III, Govindjee (ed.): Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Advances in Photosynthesis and Respiration. Pp. 631-643. Springer, Dordrecht 2014. Go to original source...
    33. Demmig-Adams B., Stewart J.J., Adams W.W. III: Environmental regulation of intrinsic photosynthetic capacity: an integrated view. - Curr. Opin. Plant Biol. 37: 34-41, 2017. Go to original source...
    34. Demmig-Adams B., Stewart J.J., Baker C.R., Adams W.W. III: Optimization of photosynthetic productivity in contrasting environments by regulons controlling plant form and function. - Int. J. Mol. Sci. 19: 872, 2018. Go to original source...
    35. Dhayalan V., Karuppasamy S.: Plant growth promoting rhizobacteria in promoting sustainable agriculture. - Global J. Environ. Sci. Manage. 7: 1-18, 2021.
    36. Diaz C., Purdy S., Christ A. et al.: Characterization of markers to determine the extent and variability of leaf senescence in Arabidopsis. A metabolic profiling approach. - Plant Physiol. 138: 898-908, 2005. Go to original source...
    37. Dodds W.K., Zeglin L.H., Ramos R.J. et al.: Connections and feedback: Aquatic, plant, and soil microbiomes in heterogeneous and changing environments. - BioScience 70: 548-562, 2020. Go to original source...
    38. Du S., Zhang Y., Lin X. et al.: Regulation of nitrate reductase by nitric oxide in Chinese cabbage pakchoi (Brassica chinensis L.). - Plant Cell Environ. 31: 195-204, 2008. Go to original source...
    39. Dusenge M.E., Duarte A.G., Way D.A.: Plant carbon metabolism and climate change: Elevated CO2 and temperature impacts on photosynthesis, photorespiration and respiration. - New Phytol. 221: 32-49, 2019. Go to original source...
    40. Dyson B.C., Allwood J.W., Feil R. et al.: Acclimation of metabolism to light in Arabidopsis thaliana: the glucose 6-phosphate/phosphate translocator GPT2 directs metabolic acclimation. - Plant Cell Environ. 38: 1404-1417, 2015. Go to original source...
    41. Feng Z., Rütting T., Pleijel H. et al.: Constraints to nitrogen acquisition of terrestrial plants under elevated CO2. - Glob. Change Biol. 21: 3152-3168, 2015. Go to original source...
    42. Fester T., Giebler J., Wick L.Y. et al.: Plant-microbe interactions as drivers of ecosystem functions relevant for the biodegradation of organic contaminants. - Curr. Opin. Biotech. 27: 168-175, 2014. Go to original source...
    43. Foyer C.H.: Reactive oxygen species, oxidative signaling and the regulation of photosynthesis. - Environ. Exp. Bot. 154: 134-142, 2018. Go to original source...
    44. Foyer C.H., Noctor G.: Redox regulation in photosynthetic organisms: Signaling, acclimation, and practical implications. -Antioxid. Redox Sign. 11: 861-905, 2009. Go to original source...
    45. Foyer C.H., Noctor G.: Stress-triggered redox signalling: What's in pROSpect? - Plant Cell Environ. 39: 951-964, 2016. Go to original source...
    46. Foyer C.H., Noctor G.: Redox homeostasis and signaling in a higher-CO2 world. - Annu. Rev. Plant Biol. 71: 157-182, 2020. Go to original source...
    47. Fuller A.W., Young P., Pierce B.D. et al.: Redox-mediated quorum sensing in plants. - PLoS ONE 12: e0182655, 2017. Go to original source...
    48. Gavito M.E., Bruhn D., Jakobsen I.: Phosphorus uptake by arbuscular mycorrhizal hyphae does not increase when the host plant grows under atmospheric CO2 enrichment. - New Phytol. 154: 751-760, 2002. Go to original source...
    49. Gavito M.E., Jakobsen I., Mikkelsen T.N., Mora F.: Direct evidence for modulation of photosynthesis by an arbuscular mycorrhiza-induced carbon sink strength. - New Phytol. 223: 896-907, 2019. Go to original source...
    50. Gill T.P.: The global epidemic of obesity. - Asia Pac. J. Clin. Nutr. 8: 75-81, 1999. Go to original source...
    51. Grant A., People J., Rémond M. et al.: How a host cell signalling molecule modifies carbon metabolism in symbionts of the coral Plesiastrea versipora. - FEBS J. 280: 2085-2096, 2013. Go to original source...
    52. Grant A., Rémond M., Starke-Peterkovic T., Hinde R.: A cell signal from the coral Plesiastrea versipora reduces starch synthesis in its symbiotic alga, Symbiodinium sp. - Comp. Biochem. Physiol. A 144: 458-463, 2006. Go to original source...
    53. Han B., Lin C.C.J., Hu G., Wang M.C.: 'Inside Out'- a dialogue between mitochondria and bacteria. - FEBS J. 286: 630-641, 2019. Go to original source...
    54. Hasanuzzaman M., Bhuyan M.H.M.B., Parvin K. et al.: Regulation of ROS metabolism in plants under environmental stress: A review of recent experimental evidence. - Int. J. Mol. Sci. 21: 8695, 2020. Go to original source...
    55. Havaux M., García-Plazaola J.I.: Beyond non-photochemical fluorescence quenching: the overlapping antioxidant functions of zeaxanthin and tocopherols. - In: Demmig-Adams B., Garab G., Adams W.W. III, Govindjee (ed.): Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Advances in Photosynthesis and Respiration. Pp. 583-603. Springer, Dordrecht 2014. Go to original source...
    56. Hu Y., Fan L., Liu Z. et al.: Rice production and climate change in Northeast China: Evidence of adaptation through land use shifts. - Environ. Res. Lett. 14: 024014, 2019. Go to original source...
    57. Huang W., Gilbert S., Poulev A. et al.: Host-specific and tissue-dependent orchestration of microbiome community structure in traditional rice paddy ecosystems. - Plant Soil 452: 379-395, 2020. Go to original source...
    58. Ishizawa H., Kuroda M., Inoue D. et al.: Community dynamics of duckweed-associated bacteria upon inoculation of plant growth-promoting bacteria. - FEMS Microbiol. Ecol. 96: fiaa101, 2020. Go to original source...
    59. Ishizawa H., Kuroda M., Morikawa M., Ike M.: Evaluation of environmental bacterial communities as a factor affecting the growth of duckweed Lemna minor. - Biotechnol. Biofuels 10: 62, 2017. Go to original source...
    60. Islam M.S., Kormoker T., Idris A.M. et al.: Plant-microbe-metal interactions for heavy metal bioremediation: A review. - Crop Pasture Sci., 2021. (In print) Go to original source...
    61. Ivanov A.G., Rosso D., Savitch L.V. et al.: Implications of alternative electron sinks in increased resistance of PSII and PSI photochemistry to high light stress in cold-acclimated Arabidopsis thaliana. - Photosynth. Res. 113: 191-206, 2012. Go to original source...
    62. Jifon J.L., Wolfe D.W.: Photosynthetic acclimation to elevated CO2 in Phaseolus vulgaris L. is altered by growth response to nitrogen supply. - Glob. Change Biol. 8: 1018-1027, 2002. Go to original source...
    63. Johnson N.C., Wilson G.W.T., Bowker M.A. et al.: Resource limitation is a driver of local adaptation in mycorrhizal symbioses. - P. Natl. Acad. Sci. USA 107: 2093-2098, 2010. Go to original source...
    64. Kasai M.: Regulation of leaf photosynthetic rate correlating with leaf carbohydrate status and activation state of Rubisco under a variety of photosynthetic source/sink balances. - Physiol. Plantarum 134: 216-226, 2008. Go to original source...
    65. Kawashima R., Sato R., Harada K., Masuda S.: Relative contributions of PGR5- and NDH-dependent photosystem I cyclic electron flow in the generation of a proton gradient in Arabidopsis chloroplasts. - Planta 246: 1045-1050, 2017. Go to original source...
    66. Khairina Y., Jog R., Boonmak C. et al.: Indigenous bacteria, an excellent reservoir of functional plant growth promoters for enhancing duckweed biomass yield on site. - Chemosphere 268: 129247, 2021. Go to original source...
    67. Kilb B., Wietoska H., Godde D.: Changes in the expression of photosynthetic genes precede loss of photosynthetic activities and chlorophyll when glucose is supplied to mature spinach leaves. - Plant Sci. 115: 225-235, 1996. Go to original source...
    68. Kim M.J., Ciani S., Schachtman D.P.: A peroxidase contributes to ROS production during Arabidopsis root response to potassium deficiency. - Mol. Plant 3: 420-427, 2010. Go to original source...
    69. Knappe S., Flügge U.-I., Fischer K.: Analysis of the plastidic phosphate translocator gene family in Arabidopsis and identification of new phosphate translocator-homologous transporters, classified by their putative substrate-binding site. - Plant Physiol. 131: 1178-1190, 2003. Go to original source...
    70. Kramer D.M., Avenson T.J., Edwards G.E.: Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions. - Trends Plant Sci. 9: 349-357, 2004. Go to original source...
    71. Krapp A., Stitt M.: An evaluation of direct and indirect mechanisms for the "sink-regulation" of photosynthesis in spinach: Changes in gas exchange, carbohydrates, metabolites, enzyme activities and steady-state transcript levels after cold-girdling source leaves. - Planta 195: 313-323, 1995. Go to original source...
    72. Krasensky-Wrzaczek J., Kangasjärvi J.: The role of reactive oxygen species in the integration of temperature and light signals. - J. Exp. Bot. 69: 3347-3358, 2018. Go to original source...
    73. Lake J.A., Woodward F.I., Quick W.P.: Long-distance CO2 signalling in plants. - J. Exp. Bot. 53: 183-193, 2002. Go to original source...
    74. Lamhamedi M.S., Godbout C., Fortin J.A.: Dependence of Laccaria bicolor basidiome development on current photosynthesis of Pinus strobus seedlings. - Can. J. Forest Res. 24: 1797-1804, 1994. Go to original source...
    75. Li P., Ainsworth E.A., Leakey A.D.B. et al.: Arabidopsis transcript and metabolite profiles: ecotype-specific responses to open-air elevated [CO2]. - Plant Cell Environ. 31: 1673-1687, 2008. Go to original source...
    76. Logan B.A., Demmig-Adams B., Rosenstiel T.N., Adams W.W. III: Effect of nitrogen limitation on foliar antioxidants in relationship to other metabolic characteristics. - Planta 209: 213-220, 1999. Go to original source...
    77. Macabuhay A., Houshmandfar A., Nuttall J. et al.: Can elevated CO2 buffer the effects of heat waves on wheat in a dryland cropping system? - Environ. Exp. Bot. 155: 578-588, 2018. Go to original source...
    78. Marquez-Santacruz H.A., Hernandez-Leon R., Orozco-Mosqueda M.C. et al.: Diversity of bacterial endophytes in roots of Mexican husk tomato plants (Physalis ixocarpa) and their detection in the rhizosphere. - Genet. Mol. Res. 9: 2372-2380, 2010. Go to original source...
    79. Mhamdi A., Noctor G.: High CO2 primes plant biotic stress defences through redox-linked pathways. - Plant Physiol. 172: 929-942, 2016. Go to original source...
    80. Mølmann J.A.B., Dalmannsdottir S., Hykkerud A.L. et al.: Influence of Arctic light conditions on crop production and quality. - Physiol. Plantarum 172: 1931-1940, 2021. Go to original source...
    81. Moore B.D., Cheng S., Sims D., Seemann J.R.: The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2. - Plant Cell Environ. 22: 567-582, 1999. Go to original source...
    82. Mueller U.G., Sachs J.L.: Engineering microbiomes to improve plant and animal health. - Trends Microbiol. 23: 606-617, 2015. Go to original source...
    83. Ohkama-Ohtsu N., Wasaki J.: Recent progress in plant nutrition research: Cross-talk between nutrients, plant physiology and soil microorganisms. - Plant Cell Physiol. 51: 1255-1264, 2010. Go to original source...
    84. Ortíz J., Sanhueza C., Romero-Munar A. et al.: In vivo metabolic regulation of alternative oxidase under nutrient deficiency - interaction with arbuscular mycorrhizal fungi and Rhizobium bacteria. - Int. J. Mol. Sci. 21: 4201, 2020. Go to original source...
    85. Padhan B.K., Sathee L., Meena H.S. et al.: CO2 elevation accelerates phenology and alters carbon/nitrogen metabolism vis-à-vis ROS abundance in bread wheat. - Front. Plant Sci. 11: 1061, 2020. Go to original source...
    86. Paul M.J., Driscoll S.P.: Sugar repression of photosynthesis: The role of carbohydrates in signalling nitrogen deficiency through source:sink imbalance. - Plant Cell Environ. 20: 110-116, 1997. Go to original source...
    87. Paul M.J., Foyer C.H.: Sink regulation of photosynthesis. - J. Exp. Bot. 52: 1383-1400, 2001. Go to original source...
    88. Phour M., Sehrawat A., Sindhu S.S., Glick B.R.: Interkingdom signaling in plant-rhizomicrobiome interactions for sustainable agriculture. - Microbiol. Res. 241: 126589, 2020. Go to original source...
    89. Pieterse C.M.J., de Jonge R., Berendsen R.L.: The soil-borne supremacy. - Trends Plant Sci. 21: 171-173, 2016. Go to original source...
    90. Poorter H., Bühler J., van Dusschoten D. et al.: Pot size matters: a meta-analysis of the effects of rooting volume on plant growth. - Funct. Plant Biol. 39: 839-850, 2012. Go to original source...
    91. Poorter H., Remkes C., Lambers H.: Carbon and nitrogen economy of 24 wild species differing in relative growth rate. - Plant Physiol. 94: 621-627, 1990. Go to original source...
    92. Porras M.E., Lorenzo P., Medrano E. et al.: Photosynthetic acclimation to elevated CO2 concentration in a sweet pepper (Capsicum annuum) crop under Mediterranean greenhouse conditions: influence of the nitrogen source and salinity. - Funct. Plant Biol. 44: 573-586, 2017. Go to original source...
    93. Prins A., Kunert K., Foyer C.H.: Atmospheric CO2 signalling, cellular redox state and plant growth and development. - In: Foyer C.H., Faragher R., Thornalley P. (ed.): Redox Metabolism and Longevity Relationships in Animals and Plants. Pp. 203-226. Taylor & Francis, London 2009.
    94. Queval G., Issakidis-Bourguet E., Hoeberichts F.A. et al.: Conditional oxidative stress responses in the Arabidopsis photorespiratory mutant cat2 demonstrate that redox state is a key modulator of daylength-dependent gene expression, and define photoperiod as a crucial factor in the regulation of H2O2-induced cell death. - Plant J. 52: 640-657, 2007. Go to original source...
    95. Rana K.L., Kour D., Kaur T. et al.: Endophytic microbes: Biodiversity, plant growth-promoting mechanisms and potential applications for agricultural sustainability. - Antonie van Leeuwenhoek 113: 1075-1107, 2020. Go to original source...
    96. Romero-Munar A., Del-Saz N.F., Ribas-Carbó M. et al.: Arbuscular mycorrhizal symbiosis with Arundo donax decreases root respiration and increases both photosynthesis and plant biomass accumulation. - Plant Cell Environ. 40: 1115-1126, 2017. Go to original source...
    97. Roth M.S., Westcott D.J., Iwai M., Niyogi K.K.: Hexokinase is necessary for glucose-mediated photosynthesis repression and lipid accumulation in a green alga. - Commun. Biol. 2: 347, 2019. Go to original source...
    98. Saint-Georges-Chaumet Y., Attaf D., Pelletier E., Edeas M.: Targeting microbiota-mitochondria inter-talk: Microbiota control mitochondria metabolism. - Cell. Mol. Biol. 61: 121-124, 2015.
    99. Sardans J., Rivas-Ubach A., Peñuelas J.: The C:N:P stoichiometry of organisms and ecosystems in a changing world: a review and perspectives. - Perspect. Plant Ecol. Evol. Syst. 14: 33-47, 2012. Go to original source...
    100. Shapiguzov A., Vainonen J.P., Hunter K. et al.: Arabidopsis RCD1 coordinates chloroplast and mitochondrial functions through interaction with ANAC transcription factors. - eLife 8: e43284, 2019. Go to original source...
    101. Shin R., Schachtman D.P.: Hydrogen peroxide mediates plant root cell response to nutrient deprivation. - P. Natl. Acad. Sci. USA 101: 8827-8832, 2004. Go to original source...
    102. Stefan M., Munteanu N., Stoleru V. et al.: Seed inoculation with plant growth promoting rhizobacteria enhances photosynthesis and yield of runner bean (Phaseolus coccineus L.). -Sci. Hortic.-Amsterdam 151: 22-29, 2013. Go to original source...
    103. Stitt M., Krapp A.: The interaction between elevated carbon dioxide and nitrogen nutrition: The physiological and molecular background. - Plant Cell Environ. 22: 583-621, 1999. Go to original source...
    104. Strand D.D., Fisher N., Kramer D.M.: Distinct energetics and regulatory functions of the two major cyclic electron flow pathways in chloroplasts. - In: Kirchhoff H. (ed.): Chloroplasts: Current Research and Future Trends. Pp. 89-100. Caister Academic Press, Norfolk 2016.
    105. Suzuki N., Koussevitzky S., Mittler R., Miller G.: ROS and redox signalling in the response of plants to abiotic stress. - Plant Cell Environ. 35: 259-270, 2012. Go to original source...
    106. Syvertsen J.P., Graham J.H.: Phosphorus supply and arbuscular mycorrhizas increase growth and net gas exchange responses of two Citrus spp. grown at elevated [CO2]. - Plant Soil 208: 209-219, 1999. Go to original source...
    107. Tausz-Posch S., Tausz M., Bourgault M.: Elevated [CO2] effects on crops: advances in understanding acclimation, nitrogen dynamics and interactions with drought and other organisms. -Plant Biol. 22: 38-51, 2020. Go to original source...
    108. Thomas R.B., Strain B.R.: Root restriction as a factor in photosynthetic acclimation of cotton seedlings grown in elevated carbon dioxide. - Plant Physiol. 96: 627-634, 1991. Go to original source...
    109. Toyama T., Kuroda M., Ogata Y. et al.: Enhanced biomass production of duckweeds by inoculating a plant growth-promoting bacterium, Acinetobacter calcoaceticus P23, in sterile medium and non-sterile environmental waters. - Water Sci. Technol. 76: 1418-1428, 2017. Go to original source...
    110. Turner T.R., James E.K., Poole P.S.: The plant microbiome. - Genome Biol. 14: 209, 2013. Go to original source...
    111. Vacheron J., Desbrosses G., Bouffaud M.-L. et al.: Plant growth-promoting rhizobacteria and root system functioning. - Front. Plant Sci. 4: 356, 2013. Go to original source...
    112. Vandana U.K., Rajkumari J., Singha L.P. et al.: The endophytic microbiome as a hotspot of synergistic interactions, with prospects of plant growth promotion. - Biology 10: 101, 2021. Go to original source...
    113. Vishwakarma A., Bashyam L., Senthilkumaran B. et al.: Physiological role of AOX1a in photosynthesis and maintenance of cellular redox homeostasis under high light in Arabidopsis thaliana. - Plant Physiol. Bioch. 81: 44-53, 2014. Go to original source...
    114. Vishwakarma A., Tetali S.D., Selinski J. et al.: Importance of the alternative oxidase (AOX) pathway in regulating cellular redox and ROS homeostasis to optimize photosynthesis during restriction of the cytochrome oxidase pathway in Arabidopsis thaliana. - Ann. Bot.-London 116: 555-569, 2015. Go to original source...
    115. Vitt P., Havens K., Kramer A.T. et al.: Assisted migration of plants: Changes in latitudes, changes in attitudes. - Biol. Conserv. 143: 18-27, 2010. Go to original source...
    116. Voss I., Sunil B., Scheibe R., Raghavendra A.S.: Emerging concept for the role of photorespiration as an important part of abiotic stress response. - Plant Biol. 15: 713-722, 2013. Go to original source...
    117. Wang H., Zhou G.S., Jiang Y.L. et al.: Photosynthetic acclimation and leaf traits of Stipa bungeana in response to elevated CO2 under five different watering conditions. - Photosynthetica 55: 164-175, 2017. Go to original source...
    118. Wang J., Cheung M., Rasooli L. et al.: Plant respiration in a high CO2 world: How will alternative oxidase respond to future atmospheric and climatic conditions? - Can. J. Plant Sci. 94: 1091-1101, 2014. Go to original source...
    119. Wang S., Zhang Y., Ju W. et al.: Recent global decline of CO2 fertilization effects on vegetation photosynthesis. - Science 370: 1295-1300, 2020. Go to original source...
    120. Weese D.J., Heath K.D., Dentinger B.T.M., Lau J.A.: Long-term nitrogen addition causes the evolution of less-cooperative mutualists. - Evolution 69: 631-642, 2015. Go to original source...
    121. Wilson K.E., Ivanov A.G., Öquist G. et al.: Energy balance, organellar redox status, and acclimation to environmental stress. - Can. J. Bot. 84: 1355-1370, 2006. Go to original source...
    122. Wu F., Sun X., Hu X. et al.: Response of nitrogen metabolism in masson pine needles to elevated CO2. - Forests 11: 390, 2020. Go to original source...
    123. Xiang T., Lehnert E., Jinkerson R.E. et al.: Symbiont population control by host-symbiont metabolic interaction in Symbiodiniaceae-cnidarian associations. - Nat. Commun. 11: 108, 2020. Go to original source...
    124. Yamakawa Y., Jog R., Morikawa M.: Effects of co-inoculation of two different plant growth-promoting bacteria on duckweed. - Plant Growth Regul. 86: 287-296, 2018. Go to original source...
    125. Yang F., Xiao K., Pan H., Liu J.: Chloroplast: the emerging battlefield in plant-microbe interactions. - Front. Plant Sci. 12: 637853, 2021. Go to original source...
    126. Yang J., Kloepper J.W., Ryu C.-M.: Rhizosphere bacteria help plants tolerate abiotic stress. - Trends Plant Sci. 14: 1-4, 2009. Go to original source...
    127. Yang Y., Guo Y., Zhong J. et al.: Root physiological traits and transcriptome analyses reveal that root zone water retention confers drought tolerance to Opisthopappus taihangensis. - Sci. Rep.-UK 10: 2627, 2020. Go to original source...
    128. Yilmaz O., Kahraman K., Ozturk L.: Elevated carbon dioxide exacerbates adverse effects of Mg deficiency in durum wheat. - Plant Soil 410: 41-50, 2017. Go to original source...
    129. Yoshida K., Terashima I., Noguchi K.: Up-regulation of mitochondrial alternative oxidase concomitant with chloroplast over-reduction by excess light. - Plant Cell Physiol. 48: 606-614, 2007. Go to original source...
    130. Yoshida K., Watanabe C.K., Terashima I., Noguchi K.: Physiological impact of mitochondrial alternative oxidase on photosynthesis and growth in Arabidopsis thaliana. - Plant Cell Environ. 34: 1890-1899, 2011. Go to original source...
    131. Zaffagnini M., Fermani S., Marchand C.H. et al.: Redox homeostasis in photosynthetic organisms: novel and established thiol-based molecular mechanisms. - Antioxid. Redox Sign. 31: 155-210, 2019. Go to original source...

    Return to the content