Cold-modulated leaf compounds in winter triticale DH lines tolerant to freezing and Microdochium nivale infection: LC-MS and Raman study
Gabriela Gołębiowska
A * , Iwona Stawoska A and Aleksandra Wesełucha-Birczyńska B
+ Author Affiliations
- Author Affiliations
A Pedagogical University of Krakow, Institute of Biology, Podchorążych 2, Kraków 30-084, Poland.
B Faculty of Chemistry, Jagiellonian University, Gronostajowa 2, Kraków 30-387, Poland.
Functional Plant Biology 49(8) 725-741 https://doi.org/10.1071/FP21300
Submitted: 19 April 2021 Accepted: 12 March 2022 Published: 5 April 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Tolerance to freezing and seedling diseases caused by Microdochium spp. is an essential trait for the wintering of triticale (×Triticosecale Wittmack) and other cereals. Preceding multi-year studies indicate that after long-term exposure to the low temperature, cereal seedlings acquire a genotype-dependent cross-tolerance to other subsequent stresses. This paper presents the first non-gel protein profiling performed via high performance liquid chromatography coupled with Mass Spectrometry as well as Fourier Transform-Raman spectroscopy measurements performed directly on leaves of triticale seedlings growing under different conditions. The research used doubled haploid lines selected from the mapping population, with extreme tolerance/susceptibility to freezing and M. nivale infection. These non-targeted methods led to the detection of twenty two proteins cold-accumulated in the most tolerant seedlings in relation to susceptible ones, classified as involved in protein biosynthesis, response to different stimuli, energy balancing, oxidative stress response, protein modification, membrane structure and anthocyanin synthesis. Additionally, in seedlings of the most freezing- and M. nivale-tolerant line, cold-hardening caused decrease of the carotenoid and chlorophyll content. Moreover, a decrease in the band intensity typical for carbohydrates as well as an increase in the band intensity characteristic for protein compounds were detected. Both studied lines revealed a different answer to stress in the characteristics of phenolic components.
Keywords: biosynthesis, cold-acclimation, crops, cross-tolerance, energy balance, FT-Raman spectroscopy, label-free protein quantification, stress response.
References
Agarwal UP (2014) 1064 nm FT-Raman spectroscopy for investigations of plant cell walls and other biomass materials. Frontiers in Plant Science 5, 490| 1064 nm FT-Raman spectroscopy for investigations of plant cell walls and other biomass materials.Crossref | GoogleScholarGoogle Scholar | 25295049PubMed |
Agriculture and Horticulture Development Board (2021). Fusarium and microdochium in cereals. Available at https://ahdb.org.uk/knowledge-library/fusarium-and-microdochium-in-cereals
Ammar K, Mergoum M, Rajaram S (2004) The history and evolution of triticale. In ‘Triticale improvement and production’. (Ed. M Mergoum). Food and Agriculture Organisation, FAO Plant Production and Protection Paper 179. No. CIS-4898. International Maize and Wheat Improvement Center (CIMMYT)
Andreev G, Schrader B, Schulz H, Fuchs R, Popov S, Handjieva N (2001) Non-destructive NIR-FT-Raman analyses in practice. Part 1. Analyses of plants and historic textiles. Fresenius’ Journal of Analytical Chemistry 371, 1009–1017.
| Non-destructive NIR-FT-Raman analyses in practice. Part 1. Analyses of plants and historic textiles.Crossref | GoogleScholarGoogle Scholar | 11769790PubMed |
Badea A, Eudes F, Salmon D, Tuvesson S, Vrolijk A, Larsson C-T, Caig V, Huttner E, Kilian A, Laroche A (2011) Development and assessment of DArT markers in triticale. Theoretical and Applied Genetics 122, 1547–1560.
| Development and assessment of DArT markers in triticale.Crossref | GoogleScholarGoogle Scholar | 21394532PubMed |
Baranski R, Baranska M, Schulz H (2005) Changes in carotenoid content and distribution in living plant tissue can be observed and mapped in situ using NIR-FT-Raman spectroscopy. Planta 222, 448–457.
| Changes in carotenoid content and distribution in living plant tissue can be observed and mapped in situ using NIR-FT-Raman spectroscopy.Crossref | GoogleScholarGoogle Scholar | 16007452PubMed |
Bateman GL, Gutteridge RJ, Jenkyn JF, Self MM (2008) Effects of fluquinconazole and silthiofam, applied as seed treatments to single or consecutive crops of wheat, on take-all epidemic development and grain yields. Annals of Applied Biology 152, 243–254.
| Effects of fluquinconazole and silthiofam, applied as seed treatments to single or consecutive crops of wheat, on take-all epidemic development and grain yields.Crossref | GoogleScholarGoogle Scholar |
Brown M, Jayaweera D, Hunt A, Woodhall JW, Ray RV (2021) Yield losses and control by sedaxane and fludioxonil of soil-borne Rhizoctonia, Microdochium, and Fusarium species in winter wheat. Plant Disease 105, 2521–2530.
| Yield losses and control by sedaxane and fludioxonil of soil-borne Rhizoctonia, Microdochium, and Fusarium species in winter wheat.Crossref | GoogleScholarGoogle Scholar | 33439039PubMed |
Dubas E, Golebiowska G, Zur I, Wedzony M (2011) Microdochium nivale (Fr., Samuels & Hallett): cytological analysis of the infection process in triticale (×Triticosecale Wittm.). Acta Physiologiae Plantarum 33, 529–537.
| Microdochium nivale (Fr., Samuels & Hallett): cytological analysis of the infection process in triticale (×Triticosecale Wittm.).Crossref | GoogleScholarGoogle Scholar |
Dyda M, Wąsek I, Tyrka M, Wędzony M, Szechyńska-Hebda M (2019) Local and systemic regulation of PSII efficiency in triticale infected by the hemibiotrophic pathogen Microdochium nivale. Physiologia Plantarum 165, 711–727.
| Local and systemic regulation of PSII efficiency in triticale infected by the hemibiotrophic pathogen Microdochium nivale.Crossref | GoogleScholarGoogle Scholar | 29774565PubMed |
Eravuchira PJ, El-Abassy RM, Deshpande S, Matei MF, Mishra S, Tandon P, Kuhnert N, Materny A (2012) Raman spectroscopic characterization of different regioisomers of monoacyl and diacyl chlorogenic acid. Vibrational Spectroscopy 61, 10–16.
| Raman spectroscopic characterization of different regioisomers of monoacyl and diacyl chlorogenic acid.Crossref | GoogleScholarGoogle Scholar |
Farber C, Kurouski D (2018) Detection and identification of plant pathogens on maize kernels with a hand-held Raman spectrometer. Analytical Chemistry 90, 3009–3012.
| Detection and identification of plant pathogens on maize kernels with a hand-held Raman spectrometer.Crossref | GoogleScholarGoogle Scholar | 29461798PubMed |
Filek M, Łabanowska M, Kurdziel M, Wesełucha-Birczyńska A, Bednarska-Kozakiewicz E (2016) Structural and biochemical response of chloroplasts in tolerant and sensitive barley genotypes to drought stress. Journal of Plant Physiology 207, 61–72.
| Structural and biochemical response of chloroplasts in tolerant and sensitive barley genotypes to drought stress.Crossref | GoogleScholarGoogle Scholar | 27835766PubMed |
Gaudet DA (1994) Progress towards understanding interactions between cold hardiness and snow mold resistance and development of resistant cultivars. Canadian Journal of Plant Pathology 16, 241–246.
| Progress towards understanding interactions between cold hardiness and snow mold resistance and development of resistant cultivars.Crossref | GoogleScholarGoogle Scholar |
Gaudet DA, Kozub GC (1991) Screening winter wheat for resistance to cottony snow mold under controlled conditions. Canadian Journal of Plant Science 71, 957–965.
| Screening winter wheat for resistance to cottony snow mold under controlled conditions.Crossref | GoogleScholarGoogle Scholar |
Gaudet DA, Laroche A, Frick M, Huel R, Puchalski B (2003) Cold induced expression of plant defensin and lipid transfer protein transcripts in winter wheat. Physiologia Plantarum 117, 195–205.
| Cold induced expression of plant defensin and lipid transfer protein transcripts in winter wheat.Crossref | GoogleScholarGoogle Scholar |
Gaudet DA, Wang Y, Frick M, Puchalski B, Penniket C, Ouellet T, Robert L, Singh J, Laroche A (2011) Low temperature induced defence gene expression in winter wheat in relation to resistance to snow moulds and other wheat diseases. Plant Science 180, 99–110.
| Low temperature induced defence gene expression in winter wheat in relation to resistance to snow moulds and other wheat diseases.Crossref | GoogleScholarGoogle Scholar | 21421352PubMed |
Gawronska K, Gołębiowska-Pikania G (2016) The effects of cold-hardening and Microdochium nivale infection on oxidative stress and antioxidative protection of the two contrasting genotypes of winter triticale. European Food Research and Technology 242, 1267–1276.
Gołębiowska G, Wędzony M (2009) Cold-hardening of winter triticale (×Triticosecale Wittm.) results in increased resistance to pink snow mould Microdochium nivale (Fr., Samuels & Hallett) and genotype-dependent chlorophyll fluorescence modulations. Acta Physiologiae Plantarum 31, 1219–1227.
| Cold-hardening of winter triticale (×Triticosecale Wittm.) results in increased resistance to pink snow mould Microdochium nivale (Fr., Samuels & Hallett) and genotype-dependent chlorophyll fluorescence modulations.Crossref | GoogleScholarGoogle Scholar |
Gołębiowska G, Wędzony M, Płażek A (2011) The responses of pro- and antioxidative systems to cold-hardening and pathogenesis differ in triticale (×Triticosecale Wittm.) seedlings susceptible or resistant to pink snow mould (Microdochium nivale Fr., Samuels & Hallett). Journal of Phytopathology 159, 19–27.
| The responses of pro- and antioxidative systems to cold-hardening and pathogenesis differ in triticale (×Triticosecale Wittm.) seedlings susceptible or resistant to pink snow mould (Microdochium nivale Fr., Samuels & Hallett).Crossref | GoogleScholarGoogle Scholar |
Gołębiowska GJ, Bonar E, Emami K, Wędzony M (2019) Cold-modulated small proteins abundance in winter triticale (×Triticosecale, Wittm.) seedlings tolerant to the pink snow mould (Microdochium nivale, Samuels and Hallett) infection. Acta Biochimica Polonica 66, 343–350.
| Cold-modulated small proteins abundance in winter triticale (×Triticosecale, Wittm.) seedlings tolerant to the pink snow mould (Microdochium nivale, Samuels and Hallett) infection.Crossref | GoogleScholarGoogle Scholar | 31509370PubMed |
Gołębiowska-Pikania G, Golemiec E (2015) Cold-enhanced gene expression of the foliar thiol-specific antioxidant protein in triticale (×Triticosecale Wittm.) seedlings resistant to Microdochium nivale (Samuels and IC Hallett) infection. Zeszyty Naukowe Uniwersytetu Szczecińskiego. Acta Biologica 22
Gołębiowska-Pikania G, Dziurka M, Wąsek I, Wajdzik K, Dyda M, Wędzony M (2019) Changes in phenolic acid abundance involved in low temperature and Microdochium nivale (Samuels and Hallett) cross-tolerance in winter triticale (×Triticosecale Wittmack). Acta Physiologiae Plantarum 41, 1–14.
| Changes in phenolic acid abundance involved in low temperature and Microdochium nivale (Samuels and Hallett) cross-tolerance in winter triticale (×Triticosecale Wittmack).Crossref | GoogleScholarGoogle Scholar |
Heredia-Guerrero JA, Benitez JJ, Dominguez E, Bayer IS, Cingolani R, Athanassiou A, Heredia A (2014) Infrared and Raman spectroscopic features of plant cuticles: a review. Frontiers in Plant Science 5, 305
| Infrared and Raman spectroscopic features of plant cuticles: a review.Crossref | GoogleScholarGoogle Scholar | 25009549PubMed |
Hoagland DR, Arnon DI (1938) Growing plants without soil by the water-culture method. The College of Agriculture University of California, Berkeley.
Hudec K, Bokor P (2002) Field patogenicity of Fusarium culmorum, Fusarium equiseti and Microdochium nivale on triticale. Physiologia Plantarum 115, 101–110.
Humphreys J, Cooke BM, Storey T (1995) Effects of seed-borne Microdochium nivale on establishment and grain yield of winter-sown wheat. Plant Varieties & Seeds 8, 107–117.
Hura T, Dziurka M, Hura K, Ostrowska A, Dziurka K (2016) Different allocation of carbohydrates and phenolics in dehydrated leaves of triticale. Journal of Plant Physiology 202, 1–9.
| Different allocation of carbohydrates and phenolics in dehydrated leaves of triticale.Crossref | GoogleScholarGoogle Scholar | 27450489PubMed |
Jozefowicz AM, Doll S, Mock HP (2020) Proteomic approaches to identify proteins responsive to cold stress. Methods in Molecular Biology 2156, 161–170.
| Proteomic approaches to identify proteins responsive to cold stress.Crossref | GoogleScholarGoogle Scholar | 32607981PubMed |
Käll L, Storey JD, MacCoss MJ, Noble WS (2008) Posterior error probabilities and false discovery rates: two sides of the same coin. Journal of Proteome Research 7, 40–44.
| Posterior error probabilities and false discovery rates: two sides of the same coin.Crossref | GoogleScholarGoogle Scholar | 18052118PubMed |
Kawakami A, Yoshida M (2012) Graminan breakdown by fructan exohydrolase induced in winter wheat inoculated with snow mold. Journal of Plant Physiology 169, 294–302.
| Graminan breakdown by fructan exohydrolase induced in winter wheat inoculated with snow mold.Crossref | GoogleScholarGoogle Scholar | 21983139PubMed |
Kolupaev YE, Horielova EI, Yastreb TO, Ryabchun NI (2020) State of antioxidant system in triticale seedlings at cold hardening of varieties of different frost resistance. Cereal Research Communications 48, 165–171.
| State of antioxidant system in triticale seedlings at cold hardening of varieties of different frost resistance.Crossref | GoogleScholarGoogle Scholar |
Kuwabara C, Takezawa D, Shimada T, Hamada T, Fujikawa S, Arakawa K (2002) Abscisic acid- and cold-induced thaumatin-like protein in winter wheat has an antifungal activity against snow mould, Microdochium nivale. Physiologia Plantarum 115, 101–110.
| Abscisic acid- and cold-induced thaumatin-like protein in winter wheat has an antifungal activity against snow mould, Microdochium nivale.Crossref | GoogleScholarGoogle Scholar | 12010473PubMed |
Leroux P, Walker AS, Albertini C, Gredt M (2006) Resistance to fungicides in French populations of Septoria tritici, the causal agent of wheat leaf blotch. Aspects of Applied Biology 78, 153–162.
Lukaszewski AJ (2003) Registration of three germplasms of hexaploid triticale with introgressions of wheat storage protein loci from chromosome 1D of bread wheat. Crop Science 43, 2316–2316.
| Registration of three germplasms of hexaploid triticale with introgressions of wheat storage protein loci from chromosome 1D of bread wheat.Crossref | GoogleScholarGoogle Scholar |
Machczyńska J, Zimny J, Bednarek PT (2015) Tissue culture-induced genetic and epigenetic variation in triticale (×Triticosecale spp. Wittmack ex A. Camus 1927) regenerants. Plant Molecular Biology 89, 279–292.
| Tissue culture-induced genetic and epigenetic variation in triticale (×Triticosecale spp. Wittmack ex A. Camus 1927) regenerants.Crossref | GoogleScholarGoogle Scholar | 26337939PubMed |
Marzec-Schmidt K, Hura K, Płażek A (2018) Changes in antioxidants activity in grasses from complex Lolium-Festuca as a response to Microdochium nivale infection. Physiological and Molecular Plant Pathology 104, 40–47.
| Changes in antioxidants activity in grasses from complex Lolium-Festuca as a response to Microdochium nivale infection.Crossref | GoogleScholarGoogle Scholar |
Matsumoto N, Hsiang T (2016) ‘Snow Mold: the battle under snow between fungal pathogens and their plant hosts.’ (Springer)
Mergoum M, Singh PK, Pena RJ, Lozano-del Río AJ, Cooper KV, Salmon DF, Macpherson HG (2009) Triticale: a “new” crop with old challenges. In ‘Cereals’. (Ed. M Carena) pp. 267–287. (Springer: New York, NY)
Mergoum M, Sapkota S, El Doliefy AEA, Naraghi SM, Pirseyedi S, Alamri MS, Abu Hammad W (2019) Triticale (×Triticosecale Wittmack) breeding. In ‘Advances in plant breeding strategies: cereals’. (Eds J Al-Khayri, S Jain, D Johnson) pp. 405–451. (Springer: Cham)
Miedaner T, Höxter H, Geiger HH (1993) Development of a resistance test for winter rye to snow mold (Microdochium nivale) under controlled environment conditions in regard to field inoculations. Canadian Journal of Botany 71, 136–144.
| Development of a resistance test for winter rye to snow mold (Microdochium nivale) under controlled environment conditions in regard to field inoculations.Crossref | GoogleScholarGoogle Scholar |
Muik B, Lendl B, Molina-Diaz A, Ayora-Canada MJ (2005) Direct monitoring of lipid oxidation in edible oils by Fourier transform Raman spectroscopy. Chemistry and Physics of Lipids 134, 173–182.
| Direct monitoring of lipid oxidation in edible oils by Fourier transform Raman spectroscopy.Crossref | GoogleScholarGoogle Scholar | 15784235PubMed |
Nakajima T, Abe J (1996) Environmental factors affecting expression of resistance to pink snow mold caused by Microdochium nivale in winter wheat. Canadian Journal of Botany 74, 1783–1788.
| Environmental factors affecting expression of resistance to pink snow mold caused by Microdochium nivale in winter wheat.Crossref | GoogleScholarGoogle Scholar |
Niedziela A, Bednarek PT, Cichy H, Budzianowski G, Kilian A, Anioł A (2012) Aluminum tolerance association mapping in triticale. BMC Genomics 13, 67
| Aluminum tolerance association mapping in triticale.Crossref | GoogleScholarGoogle Scholar | 22330691PubMed |
Nielsen AV, Tetens I, Meyer AS (2013) Potential of phytase-mediated iron release from cereal-based foods: a quantitative view. Nutrients 5, 3074–3098.
| Potential of phytase-mediated iron release from cereal-based foods: a quantitative view.Crossref | GoogleScholarGoogle Scholar | 23917170PubMed |
Oliwa J, Stawoska I, Janeczko A, Okleštková J, Skoczowski A (2019) Response of the photosynthetic apparatus in the tropical fern Platycerium bifurcatum to increased ozone concentration. Photosynthetica 57, 1119–1129.
| Response of the photosynthetic apparatus in the tropical fern Platycerium bifurcatum to increased ozone concentration.Crossref | GoogleScholarGoogle Scholar |
Ponomareva ML, Gorshkov VY, Ponomarev SN, Korzun V, Miedaner T (2020) Snow mold of winter cereals: a complex disease and a challenge for resistance breeding. Theoretical and Applied Genetics 134, 419–433.
| Snow mold of winter cereals: a complex disease and a challenge for resistance breeding.Crossref | GoogleScholarGoogle Scholar | 33221940PubMed |
Rapacz M, Sasal M, Gut M (2011) Chlorophyll fluorescence-based studies of frost damage and the tolerance for cold-induced photoinhibition in freezing tolerance analysis of Triticale (×Triticosecale Wittmack). Journal of Agronomy and Crop Science 197, 378–389.
| Chlorophyll fluorescence-based studies of frost damage and the tolerance for cold-induced photoinhibition in freezing tolerance analysis of Triticale (×Triticosecale Wittmack).Crossref | GoogleScholarGoogle Scholar |
Rapacz M, Sasal M, Kalaji HM, Kościelniak J (2015) Is the OJIP test a reliable indicator of winter hardiness and freezing tolerance of common wheat and triticale under variable winter environments. PLoS ONE 10, e013482
| Is the OJIP test a reliable indicator of winter hardiness and freezing tolerance of common wheat and triticale under variable winter environments.Crossref | GoogleScholarGoogle Scholar |
Rys M, Szaleniec M, Skoczowski A, Stawoska I, Janeczko A (2015) FT-Raman spectroscopy as a tool in evaluation the response of plants to drought stress. Open Chemistry 13, 1091–1100.
| FT-Raman spectroscopy as a tool in evaluation the response of plants to drought stress.Crossref | GoogleScholarGoogle Scholar |
Schrader B, Klump HH, Schenzel K, Schulz H (1999) Non-destructive NIR FT Raman analysis of plants. Journal of Molecular Structure 509, 201–212.
| Non-destructive NIR FT Raman analysis of plants.Crossref | GoogleScholarGoogle Scholar |
Schulz H (2014) Qualitative and quantitative FT-Raman analysis of plants. In ‘Optical spectroscopy and computational methods in biology and medicine’. (Ed. M Baranska). pp. 253–278. (Springer Netherlands: Dordrecht)
Schulz H, Baranska M (2007) Identification and quantification of valuable plant substances by IR and Raman spectroscopy. Vibrational Spectroscopy 43, 13–25.
| Identification and quantification of valuable plant substances by IR and Raman spectroscopy.Crossref | GoogleScholarGoogle Scholar |
Sliesaravičius A, Pekarskas J, Rutkovienė V, Baranauskis K (2006) Grain yield and disease resistance of winter cereal varieties and application of biological agent in organic agriculture. Agronomy Research 4, 371–378.
Stawoska I, Wesełucha-Birczyńska A, Regonesi ME, Riva M, Tortora P, Stochel G (2009) Interaction of selected divalent metal ions with human ataxin-3 Q36. Journal of Biological Inorganic Chemistry 14, 1175–1185.
| Interaction of selected divalent metal ions with human ataxin-3 Q36.Crossref | GoogleScholarGoogle Scholar | 19575245PubMed |
Stawoska I, Staszak AM, Ciereszko I, Oliwa J, Skoczowski A (2020) Using isothermal calorimetry and FT-Raman spectroscopy for step-by-step monitoring of maize seed germination: case study. Journal of Thermal Analysis and Calorimetry 142, 755–763.
| Using isothermal calorimetry and FT-Raman spectroscopy for step-by-step monitoring of maize seed germination: case study.Crossref | GoogleScholarGoogle Scholar |
Strang EJP, Eklund M, Rosenfelder P, Htoo JK, Mosenthin R (2016) Protein value of eight triticale genotypes for pigs based on standardized ileal amino acid digestibility. Journal of Animal Science 94, 457–457.
| Protein value of eight triticale genotypes for pigs based on standardized ileal amino acid digestibility.Crossref | GoogleScholarGoogle Scholar |
Szechyńska-Hebda M, Wędzony M, Tyrka M, Gołębiowska G, Chrupek M, Czyczyło-Mysza I, Dubas E, Żur I, Golemiec E (2011) Identifying QTLs for cold-induced resistance to Microdochium nivale in winter triticale. Plant Genetic Resources 9, 296–299.
| Identifying QTLs for cold-induced resistance to Microdochium nivale in winter triticale.Crossref | GoogleScholarGoogle Scholar |
Szechyńska-Hebda M, Hebda M, Mierzwiński D, Kuczyńska P, Mirek M, Wędzony M, Van Lammeren A, Karpiński S (2013) Effect of cold-induced changes in physical and chemical leaf properties on the resistance of winter triticale (×Triticosecale) to the fungal pathogen Microdochium nivale. Plant Pathology 62, 867–878.
| Effect of cold-induced changes in physical and chemical leaf properties on the resistance of winter triticale (×Triticosecale) to the fungal pathogen Microdochium nivale.Crossref | GoogleScholarGoogle Scholar |
Tarkowski C (1989) ‘Biologia pszenżyta [Triticale biology].’ (PWN Warszawa) [in Polish].
Thygesen LG, Lokke MM, Micklander E, Engelsen SB (2003) Vibrational microspectroscopy of food. Raman vs. FT-IR. Trends in Food Science and Technology 14, 50–57.
| Vibrational microspectroscopy of food. Raman vs. FT-IR.Crossref | GoogleScholarGoogle Scholar |
Tronsmo AM, Hsiang T, Okuyama H, Nakajima T (2001) Low temperature diseases caused by Microdochium nivale. In ‘Low temperature plant microbe interactions under snow’. (Ed. N Iriki, DA Gaudet, AM Tronsmo, N Matsumoto, M Yoshida, A Nishimune) pp. 75–86. (Hokkaido National Agricultural Experimental Station: Sapporo)
Tyrka M, Chełkowski J (2004) Enhancing the resistance of triticale by using genes from wheat and rye. Journal of Applied Genetics 45, 283–295.
Vitek P, Novotna K, Hodanova P, Rapantova B, Klem K (2017) Detection of herbicide effects on pigment composition and PSII photochemistry in Helianthus annuus by Raman spectroscopy and chlorophyll a fluorescence. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 170, 234–241.
| Detection of herbicide effects on pigment composition and PSII photochemistry in Helianthus annuus by Raman spectroscopy and chlorophyll a fluorescence.Crossref | GoogleScholarGoogle Scholar |
Wąsek I, Dyda M, Gołębiowska G, Tyrka M, Rapacz M, Szechyńska-Hebda M, Wędzony M (2021) Quantitative trait loci and candidate genes associated with freezing tolerance of winter triticale (×Wittmack). Journal of Applied Genetics 63, 15–33.
| Quantitative trait loci and candidate genes associated with freezing tolerance of winter triticale (×Wittmack).Crossref | GoogleScholarGoogle Scholar | 34491554PubMed |
Wędzony M (2003) Protocol for anther culture in hexaploid triticale (×Triticosecale Wittm.). In ‘Doubled haploid production in crop plants’. (Eds M Maluszynski, KJ Kasha, BP Forster, I Szarejko) pp. 123–128. (Springer: Dordrecht)
Wesełucha-Birczyńska A, Łabanowska M, Kurdziel M, Filek M (2012) Resonance Raman and EPR spectroscopy studies of untreated spring wheat leaves. Vibrational Spectroscopy 60, 113–117.
| Resonance Raman and EPR spectroscopy studies of untreated spring wheat leaves.Crossref | GoogleScholarGoogle Scholar |
Withnall R, Chowdhry BZ, Silver J, Edwards HGM, de Oliveira LFC (2003) Raman spectra of carotenoids in natural products. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 59, 2207–2212.
| Raman spectra of carotenoids in natural products.Crossref | GoogleScholarGoogle Scholar |
Yeh S, Moffatt BA, Griffith M, Xiong F, Yang DS, Wiseman SB, Sarhan F, Danyluk J, Xue YQ, Hew CL, Doherty-Kirby A, Lajoie G (2000) Chitinase genes responsive to cold encode antifreeze proteins in winter cereals. Plant physiology 124, 1251–1264.
| Chitinase genes responsive to cold encode antifreeze proteins in winter cereals.Crossref | GoogleScholarGoogle Scholar | 11080301PubMed |
Zhukovsky A, Ilyuk A (2010) Snow mould harmfulness in winter triticale and the efficiency of seed dressing products in the Republic of Belarus. Progress in Plant Protection 50, 1841–1846.
Żur I, Gołębiowska G, Dubas E, Golemiec E, Matušíková I, Libantová J, Moravčíková J (2013) β-1,3-glucanase and chitinase activities in winter triticales during cold hardening and subsequent infection by Microdochium nivale. Biologia 68, 241–248.
| β-1,3-glucanase and chitinase activities in winter triticales during cold hardening and subsequent infection by Microdochium nivale.Crossref | GoogleScholarGoogle Scholar |
