The metabolic response of Araucaria angustifolia embryogenic cells to heat stress is associated with their maturation potential
Fernando Diego Kaziuk A # , Ana Luiza Dorigan de Matos Furlanetto A # , André Luis Wendt dos Santos B , Eny Iochevet Senegal Floh B , Lucelia Donatti C , Maria Eliane Merlin Rocha A , Fabiane Fortes D , Glaucia Regina Martinez A and Silvia Maria Suter Correia Cadena A *A
B
C
D
Handling Editor: Manuela Chaves
Abstract
Araucaria angustifolia is a critically endangered species and its distribution can be affected by an increase in temperature. In this study, we evaluated the effects of heat stress (30°C) on Araucaria angustifolia cell lines responsive (SE1) and non-responsive (SE6) to the development of somatic embryos. The viability of both cell lines was reduced by heat stress and mitochondria were the organelles most affected. Heat stress for 24 h increased the reactive oxygen species (ROS) levels in SE1 cells, followed by a reduction at 48 and 72 h. In SE6 cells, an increase occurred after 24 and 48 h of stress, returning to control levels at 72 h. H2O2 levels were increased after 24 h for both SE1 and SE6 cells, being higher for SE6. Interestingly, at 48 and 72 h, H2O2 levels decreased in SE1 cells, while in SE6, the values returned to the control levels. The respiration of SE6 cells in the presence of oxidisable substrates was inhibited by heat stress, in agreement with the high lipid peroxidation levels. The AaSERK1 gene was identified in both cultures, with greater expression in the SE1 line. Heat stress for 24 and 48 h increased gene expression only in this cell line. The activity of peroxidase, superoxide dismutase and enzymes of the glutathione/ascorbate cycle was increased in both cell lines subjected to heat stress. Catalase activity was increased only in SE6 cells at 72 h of exposure. These results show that responsive SE1 cells can modulate ROS levels more efficiently than SE6 when these cells are stressed by heat. This ability may be related to the maturation capacity of these cells.
Keywords: Araucaria angustifolia, bioenergetics, heat stress, maturation, metabolic response, oxidative stress, redox balance, somatic embryogenesis.
References
Abiko M, Akibayashi K, Sakata T, Kimura M, Kihara M, Itoh K, Asamizu E, Sato S, Takahashi H, Higashitani A (2005) High-temperature induction of male sterility during barley (Hordeum vulgare L.) anther development is mediated by transcriptional inhibition. Sexual Plant Reproduction 18, 91-100.
| Crossref | Google Scholar |
Aebi H (1984) [13] Catalase in vitro. Methods in Enzymology 105, 121–-126.
| Crossref | Google Scholar |
Ahuja I, de Vos RCH, Bones AM, Hall RD (2010) Plant molecular stress responses face climate change. Trends in Plant Science 15, 664-674.
| Crossref | Google Scholar | PubMed |
Almeselmani M, Deshmukh PS, Sairam RK, Kushwaha SR, Singh TP (2006) Protective role of antioxidant enzymes under high temperature stress. Plant Science 171, 382-388.
| Crossref | Google Scholar | PubMed |
Astarita LV, Guerra MP (2000) Conditioning of the culture medium by suspension cells and formation of somatic proembryo in Araucaria angustifolia (coniferae). In Vitro Cellular & Developmental Biology – Plant 36, 194-200.
| Crossref | Google Scholar |
Becwar MR, Noland TL, Wyckoff JL (1989) Maturation, germination, and conversion of norway spruce (Picea abies L.) somatic embryos to plants. In Vitro Cellular & Developmental Biology 25, 575-580.
| Crossref | Google Scholar |
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248-254.
| Crossref | Google Scholar | PubMed |
Castander-Olarieta A, Montalbán IA, De Medeiros Oliveira E, Dell’Aversana E, D’Amelia L, Carillo P, Steiner N, Fraga HPDF, Guerra MP, Goicoa T, Ugarte MD, Pereira C, Moncaleán P (2019) Effect of thermal stress on tissue ultrastructure and metabolite profiles during initiation of radiata pine somatic embryogenesis. Frontiers in Plant Science 9, 2004.
| Crossref | Google Scholar |
Chen B, Li C, Chen Y, Chen S, Xiao Y, Wu Q, Zhong L, Huang K (2022) Proteome profiles during early stage of somatic embryogenesis of two Eucalyptus species. BMC Plant Biology 22, 558.
| Crossref | Google Scholar |
Czarnocka W, Karpiński S (2018) Friend or foe? Reactive oxygen species production, scavenging and signaling in plant response to environmental stresses. Free Radical Biology and Medicine 122, 4-20.
| Crossref | Google Scholar | PubMed |
Dorigan de Matos Furlanetto AL, Valente C, Martinez GR, Merlin Rocha ME, Maurer JBB, Cadena SMSC (2019) Cold stress on Araucaria angustifolia embryogenic cells results in oxidative stress and induces adaptation: implications for conservation and propagation. Free Radical Research 53, 45-56.
| Crossref | Google Scholar | PubMed |
Dorigan de Matos Furlanetto AL, Kaziuk FD, Martinez GR, Donatti L, Merlin Rocha ME, dos Santos ALW, Floh EIS, Cadena SMSC (2021) Mitochondrial bioenergetics and enzymatic antioxidant defense differ in Paraná pine cell lines with contrasting embryogenic potential. Free Radical Research 55, 255-266.
| Crossref | Google Scholar |
dos Santos ALW, Steiner N, Guerra MP, Zoglauer K, Moerschbacher BM (2008) Somatic embryogenesis in Araucaria angustifolia. Biologia Plantarum 52, 195-199.
| Crossref | Google Scholar |
dos Santos ALW, Jo L, Santa-Catarina C, Guerra MP, Floh EIS (2012) Somatic embryogenesis in Brazilian pine: establishment of biochemical markers for selection of cell lines with high embryogenic potential. In ‘Integrating vegetative propagation, biotechnologies and genetic improvement for tree production and sustainable forest management’. p. 243. (Instituto de Biociências, Universidade de São Paulo)
dos Santos ALW, Elbl P, Navarro BV, de Oliveira LF, Salvato F, Balbuena TS, Floh EIS (2016) Quantitative proteomic analysis of Araucaria angustifolia (Bertol.) Kuntze cell lines with contrasting embryogenic potential. Journal of Proteomics 130, 180-189.
| Crossref | Google Scholar |
Elbl P, Lira BS, Andrade SCS, Jo L, dos Santos ALW, Coutinho LL, Floh EIS, Rossi M (2015) Comparative transcriptome analysis of early somatic embryo formation and seed development in Brazilian pine, Araucaria angustifolia (Bertol.) Kuntze. Plant Cell, Tissue and Organ Culture (PCTOC) 120, 903-915.
| Crossref | Google Scholar |
Foyer CH (2018) Reactive oxygen species, oxidative signaling and the regulation of photosynthesis. Environmental and Experimental Botany 154, 134-142.
| Crossref | Google Scholar | PubMed |
Fritzsons E, Wrege MS, Mantovani LE (2018) Climatic aspects related to the distribution of Brazilian pine in the state of Santa Catarina. Floresta 48, 503.
| Crossref | Google Scholar |
Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Experimental Cell Research 50, 151-158.
| Crossref | Google Scholar | PubMed |
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48, 909-930.
| Crossref | Google Scholar |
GISTEMP Team (2023) GISS Surface Temperature Analysis (GISTEMP), version 4. NASA Goddard Institute for Space Studies. Dataset accessed 25 July 2023 at https://data.giss.nasa.gov/gistemp/. Available at https://data.giss.nasa.gov/gistemp/ [Accessed 24 July 2023]
Gulzar B, Mujib A, Malik MQ, Sayeed R, Mamgain J, Ejaz B (2020) Genes, proteins and other networks regulating somatic embryogenesis in plants. Journal of Genetic Engineering and Biotechnology 18, 31.
| Crossref | Google Scholar | PubMed |
Gupta PK, Durzan DJ (1987) Biotechnology of somatic polyembryogenesis and plantlet regeneration in loblolly pine. Bio/Technology 5, 147-151.
| Crossref | Google Scholar |
Hasanuzzaman M, Hossain MA, Da Silva JAT, Fujita M (2012) Plant response and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. In ‘Crop stress and its management: perspectives and strategies’. (Eds B Venkateswarlu, A Shanker, C Shanker, M Maheswari) pp. 261–315. (Springer: Dordrecht, Netherlands) doi:10.1007/978-94-007-2220-0_8
Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207, 604-611.
| Crossref | Google Scholar |
Huang C-N, Cornejo MJ, Bush DS, Jones RL (1986) Estimating viability of plant protoplasts using double and single staining. Protoplasma 135, 80-87.
| Crossref | Google Scholar |
Jaleel CA, Riadh K, Gopi R, Manivannan P, Inès J, Al-Juburi HJ, Chang-Xing Z, Hong-Bo S, Panneerselvam R (2009) Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiologiae Plantarum 31, 427-436.
| Crossref | Google Scholar |
Jambunathan N (2010) Determination and detection of reactive oxygen species (ROS), lipid peroxidation, and electrolyte leakage in plants. In ‘Plant stress tolerance. Methods in Molecular Biology. Vol. 639’. (Ed. R Sunkar) pp. 292–298. (Humana Press: New York, NY, USA) doi:10.1007/978-1-60761-702-0_18
Jiang Z, Watanabe CKA, Miyagi A, Kawai-Yamada M, Terashima I, Noguchi K (2019) Mitochondrial AOX supports redox balance of photosynthetic electron transport, primary metabolite balance, and growth in arabidopsis thaliana under high light. International Journal of Molecular Sciences 20, 3067.
| Crossref | Google Scholar | PubMed |
Jo L, Dos Santos ALW, Bueno CA, Barbosa HR, Floh EIS (2014) Proteomic analysis and polyamines, ethylene and reactive oxygen species levels of Araucaria angustifolia (Brazilian pine) embryogenic cultures with different embryogenic potential. Tree Physiology 34, 94-104.
| Crossref | Google Scholar | PubMed |
Jones KH, Senft JA (1985) An improved method to determine cell viability by simultaneous staining with fluorescein diacetate-propidium iodide. Journal of Histochemistry & Cytochemistry 33, 77-79.
| Crossref | Google Scholar | PubMed |
Kaushal N, Gupta K, Bhandhari K, Kumar S, Thakur P, Nayyar H (2011) Proline induces heat tolerance in chickpea (Cicer arietinum L.) plants by protecting vital enzymes of carbon and antioxidative metabolism. Physiology and Molecular Biology of Plants 17, 203-213.
| Crossref | Google Scholar | PubMed |
Koyro HW, Ahmad P, Geissler N (2012) Abiotic stress responses in plants: an overview. In ‘Environmental adaptations and stress tolerance of plants in the era of climate change’. (Eds P Ahmad, M Prasad) pp. 1–28. (Springer: New York, NY, USA) doi:10.1007/978-1-4614-0815-4_1
Kumar S, Gupta D, Nayyar H (2012) Comparative response of maize and rice genotypes to heat stress: status of oxidative stress and antioxidants. Acta Physiologiae Plantarum 34, 75-86.
| Crossref | Google Scholar |
Lenssen NJL, Schmidt GA, Hansen JE, Menne MJ, Persin A, Ruedy R, Zyss D (2019) Improvements in the GISTEMP Uncertainty Model. Journal of Geophysical Research: Atmospheres 124, 6307-6326.
| Crossref | Google Scholar |
Liebthal M, Maynard D, Dietz K-J (2018) Peroxiredoxins and redox signaling in plants. Antioxidants and Redox Signaling 28, 609-624.
| Crossref | Google Scholar | PubMed |
Linghu G, Yu Z, Li M, Wang A, Kang Y (2023) Comparative transcriptome analysis between embryogenic and non-embryogenic callus of Davidia involucrata. Forests 14, 1256.
| Crossref | Google Scholar |
Lohani N, Singh MB, Bhalla PL (2020) High temperature susceptibility of sexual reproduction in crop plants. Journal of Experimental Botany 71, 555-568.
| Crossref | Google Scholar | PubMed |
Mansoor S, Ali Wani O, Lone JK, Manhas S, Kour N, Alam P, Ahmad A, Ahmad P (2022) Reactive oxygen species in plants: from source to sink. Antioxidants 11, 225.
| Crossref | Google Scholar |
Mantovani A, Morellato LPC, Reis MSd (2004) Fenologia reprodutiva e produção de sementes em Araucaria angustifolia (Bert.) O. Kuntze. Revista Brasileira de Botânica 27, 787-796.
| Crossref | Google Scholar |
Marchioro CA, Santos KL, Siminski A (2020) Present and future of the critically endangered Araucaria angustifolia due to climate change and habitat loss. Forestry: An International Journal of Forest Research 93, 401-410.
| Crossref | Google Scholar |
Mariano AB, Valente C, Maurer JBB, Cadena SMSC, Rocha MEM, de Oliveira MBM, Salgado I, Carnieri EGS (2008) Functional characterization of mitochondria isolated from the ancient gymnosperm Araucaria angustifolia. Plant Science 175, 701-705.
| Crossref | Google Scholar |
Mittler R (2017) ROS are good. Trends in Plant Science 22, 11-19.
| Crossref | Google Scholar | PubMed |
Miyake C, Asada K (1992) Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids. Plant and Cell Physiology 33, 541-553.
| Crossref | Google Scholar |
Monteiro G, Horta BB, Pimenta DC, Augusto O, Netto LES (2007) Reduction of 1-Cys peroxiredoxins by ascorbate changes the thiol-specific antioxidant paradigm, revealing another function of vitamin C. Proceedings of the National Academy of Sciences 104, 4886-4891.
| Crossref | Google Scholar |
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum 15, 473-497.
| Crossref | Google Scholar |
Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochemical Journal 417, 1-13.
| Crossref | Google Scholar |
Murshed R, Lopez-Lauri F, Sallanon H (2008) Microplate quantification of enzymes of the plant ascorbate-glutathione cycle. Analytical Biochemistry 383, 320-322.
| Crossref | Google Scholar | PubMed |
Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annual Review of Plant Physiology and Plant Molecular Biology 52, 561-591.
| Crossref | Google Scholar | PubMed |
Noctor G, Reichheld J-P, Foyer CH (2018) ROS-related redox regulation and signaling in plants. Seminars in Cell & Developmental Biology 80, 3-12.
| Crossref | Google Scholar | PubMed |
Nodari ES (2016) Historia de la devastación del bosque de araucaria en el sur del Brasil. Areas: Revista Internacional de Ciencias Sociales 55, 75-85.
| Google Scholar |
Pandey DK, Chaudhary B (2014) Oxidative stress responsive SERK1 gene directs the progression of somatic embryogenesis in cotton (Gossypium hirsutum L. cv. Coker 310). American Journal of Plant Sciences 05, 80-102.
| Crossref | Google Scholar |
Pirzadah TB, Malik B, Tahir I, Rehman RU, Hakeem KR, Alharby HF (2019) Aluminium stress modulates the osmolytes and enzyme defense system in Fagopyrum species. Plant Physiology and Biochemistry 144, 178-186.
| Crossref | Google Scholar | PubMed |
Porras-Murillo R, Andrade-Torres A, Solís-Ramos LY (2018) Expression analysis of two SOMATIC EMBRYOGENESIS RECEPTOR KINASE (SERK) genes during in vitro morphogenesis in Spanish cedar (Cedrela odorata L.). 3 Biotech 8, 470.
| Crossref | Google Scholar |
Qian J, Lu B, Chen H, Wang P, Wang C, Li K, Tian X, Jin W, He X, Chen H (2019) Phytotoxicity and oxidative stress of perfluorooctanesulfonate to two riparian plants: Acorus calamus and Phragmites communis. Ecotoxicology and Environmental Safety 180, 215-226.
| Crossref | Google Scholar | PubMed |
Quintero-Fabián S, Arreola R, Becerril-Villanueva E, Torres-Romero JC, Arana-Argáez V, Lara-Riegos J, Ramírez-Camacho MA, Alvarez-Sánchez ME (2019) Role of matrix metalloproteinases in angiogenesis and cancer. Frontiers in Oncology 9, 1370.
| Crossref | Google Scholar |
Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. The Journal of Cell Biology 17, 208-212.
| Crossref | Google Scholar |
Rubio MC, James EK, Clemente MR, Bucciarelli B, Fedorova M, Vance CP, Becana M (2004) Localization of superoxide dismutases and hydrogen peroxide in legume root nodules. Molecular Plant-Microbe Interactions 17, 1294-1305.
| Crossref | Google Scholar | PubMed |
Santa-Catarina C, Hanai LR, Dornelas MC, Viana AM, Floh EIS (2004) SERK gene homolog expression, polyamines and amino acids associated with somatic embryogenic competence of Ocotea catharinensis Mez. (Lauraceae). Plant Cell, Tissue and Organ Culture 79, 53-61.
| Crossref | Google Scholar |
Santa-Catarina C, Silveira V, Guerra MP, Steiner N, Macedo AA, Floh EIS, dos Santos ALW (2012) The use of somatic embryogenesis for mass clonal propagation and biochemical and physiological studies in woody plants. Current Topics in Plant Biology 13, 103-119.
| Google Scholar |
Santos MO, Aragão FJL (2009) Role of SERK genes in plant environmental response. Plant Signaling & Behavior 4, 1111-1113.
| Crossref | Google Scholar |
Santos ALWd, Silveira V, Steiner N, Vidor M, Guerra MP (2002) Somatic embryogenesis in Parana pine (Araucaria angustifolia (Bert.) O. Kuntze). Brazilian Archives of Biology and Technology 45, 97-106.
| Crossref | Google Scholar |
Shohael AM, Ali MB, Yu KW, Hahn EJ, Islam R, Paek KY (2006) Effect of light on oxidative stress, secondary metabolites and induction of antioxidant enzymes in Eleutherococcus senticosus somatic embryos in bioreactor. Process Biochemistry 41, 1179-1185.
| Crossref | Google Scholar |
Silveira V, Steiner N, Santos ALW, Nodari RO, Guerra MP (2002) Biotechnology tolls in Araucaria angustifolia conservation and improvement: inductive factors affecting somatic embryogenesis. Cropp Breeding and Applied Biotechnology 2, 463-470.
| Crossref | Google Scholar |
Silveira V, Santa-Catarina C, Tun NN, Scherer GFE, Handro W, Guerra MP, Floh EIS (2006) Polyamine effects on the endogenous polyamine contents, nitric oxide release, growth and differentiation of embryogenic suspension cultures of Araucaria angustifolia (Bert.) O. Ktze. Plant Science 171, 91-98.
| Crossref | Google Scholar |
Singh A, Prasad SM, Singh S (2019) Role of nano-powder of Azadirachta indica leaves to regulate the physiological responses and metal uptake in Triticum aestivum seedlings. Chemistry and Ecology 35, 483-499.
| Crossref | Google Scholar |
Soliman WS, Fujimori M, Tase K, Sugiyama S-I (2011) Oxidative stress and physiological damage under prolonged heat stress in C3 grass Lolium perenne. Grassland Science 57, 101-106.
| Crossref | Google Scholar |
Song L, Ding W, Zhao M, Sun B, Zhang L (2006) Nitric oxide protects against oxidative stress under heat stress in the calluses from two ecotypes of reed. Plant Science 171, 449-458.
| Crossref | Google Scholar | PubMed |
Stefenon VM, Klabunde G, Lemos RPM, Rogalski M, Nodari RO (2019) Phylogeography of plastid DNA sequences suggests post-glacial southward demographic expansion and the existence of several glacial refugia for Araucaria angustifolia. Scientific Reports 9, 2752.
| Crossref | Google Scholar |
Steiner N, Vieira FdN, Maldonado S, Guerra MP (2005) Effect of carbon source on morphology and histodifferentiation of Araucaria angustifolia embryogenic cultures. Brazilian Archives of Biology and Technology 48, 895-903.
| Crossref | Google Scholar |
Steiner N, Santa-Catarina C, Guerra MP, Cutri L, Dornelas MC, Floh EIS (2012) A gymnosperm homolog of SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE-1 (SERK1) is expressed during somatic embryogenesis. Plant Cell, Tissue and Organ Culture (PCTOC) 109, 41-50.
| Crossref | Google Scholar |
Suzuki N, Katano K (2018) Coordination between ROS regulatory systems and other pathways under heat stress and pathogen attack. Frontiers in Plant Science 9, 490.
| Crossref | Google Scholar |
Talapatra S, Ghoshal N, Raychaudhuri SS (2014) Molecular characterization, modeling and expression analysis of a somatic embryogenesis receptor kinase (SERK) gene in Momordica charantia L. during somatic embryogenesis. Plant Cell, Tissue and Organ Culture (PCTOC) 116, 271-283.
| Crossref | Google Scholar |
Thomas P (2013) Araucaria angustifolia. The IUCN Red List of Threatened Species e.T32975A2. Available at https://www.iucnredlist.org/species/32975/2829141
Valente C, Pasqualim P, Jacomasso T, Maurer JBB, Souza EMd, Martinez GR, Rocha MEM, Carnieri EGS, Cadena SMSC (2012) The involvement of PUMP from mitochondria of Araucaria angustifolia embryogenic cells in response to cold stress. Plant Science 197, 84-91.
| Crossref | Google Scholar |
Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Science 164, 645-655.
| Crossref | Google Scholar |
Wang X-D, Nolan KE, Irwanto RR, Sheahan MB, Rose RJ (2011) Ontogeny of embryogenic callus in Medicago truncatula: the fate of the pluripotent and totipotent stem cells. Annals of Botany 107, 599-609.
| Crossref | Google Scholar |
Wang Y, Li H-L, Zhou Y-K, Guo D, Zhu J-H, Peng S-Q (2021) Transcriptomes analysis reveals novel insight into the molecular mechanisms of somatic embryogenesis in Hevea brasiliensis. BMC Genomics 22, 183.
| Crossref | Google Scholar |
Wrege MS, Higa RCV, Britez RM, Garrastazu MC, de Sousa VA, Caramori PH, Radin B, Braga HJ (2009) Climate change and conservation of Araucaria angustifolia in Brazil. Unasylva 60, 30-33.
| Google Scholar |
Wu A, Allu AD, Garapati P, Siddiqui H, Dortay H, Zanor M-I, Asensi-Fabado MA, Munne-Bosch S, Antonio C, Tohge T, Fernie AR, Kaufmann K, Xue G-P, Mueller-Roeber B, Balazadeh S (2012) JUNGBRUNNEN1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in Arabidopsis. The Plant Cell 24, 482-506.
| Crossref | Google Scholar | PubMed |
Zandalinas SI, Mittler R, Balfagón D, Arbona V, Gómez-Cadenas A (2018) Plant adaptations to the combination of drought and high temperatures. Physiologia Plantarum 162, 2-12.
| Crossref | Google Scholar | PubMed |