Skip to main content
Log in

QTLs for cell wall-bound phenolics in relation to the photosynthetic apparatus activity and leaf water status under drought stress at different growth stages of triticale

  • Original Article
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

The present study aimed at identifying the regions of triticale genome responsible for cell wall saturation with phenolic compounds under drought stress during vegetative and generative growth. Moreover, the loci determining the activity of the photosynthetic apparatus, leaf water content (LWC) and osmotic potential (Ψ o) were identified, as leaf hydration and functioning of the photosynthetic apparatus under drought are associated with the content of cell wall-bound phenolics (CWPh). Compared with LWC and Ψ o, CWPh fluctuations were more strongly associated with changes in chlorophyll fluorescence. At the vegetative stage, CWPh fluctuations were due to the activity of three loci, of which only QCWPh.4B was also related to changes in F v/F m and ABS/CSm. In the other QTLs (QCWPh.6R.2 and QCWPh.6R.3), the genes of these loci determined also the changes in majority of chlorophyll fluorescence parameters. At the generative stage, the changes in CWPh in loci QCWPh.4B, QCWPh.3R and QCWPh.6R.1 corresponded to those in DIo/CSm. The locus QCWPh.6R.3, active at V stage, controlled majority of chlorophyll fluorescence parameters. This is the first study on mapping quantitative traits in triticale plants exposed to drought at different stages of development, and the first to present the loci for cell wall-bound phenolics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alheit KV, Reif JC, Maurer HP, Hahn V, Weissmann EA, Miedaner T, Würschum T (2011) Detection of segregation distortion loci in triticale (x Triticosecale Wittmack) based on a high-density DArT marker consensus genetic linkage map. BMC Genom 12:380

    Article  CAS  Google Scholar 

  • Barber J, Andersson B (1991) Light can be both good and bed for photosynthesis. Trends Biochem Sci 17:61–66

    Article  Google Scholar 

  • Bartrina I, Otto E, Strnad M, Werner T, Schmülling T (2011) Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. Plant Cell 23:69–80

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bilger W, Johnsen T, Schreiber U (2001) UV-excited chlorophyll fluorescence as a tool for the assessment of UV-protection by the epidermis of plants. J Exp Bot 52:2007–2014

    Article  CAS  PubMed  Google Scholar 

  • Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179–194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cvikrová M, Malá J, Hrubcová M, Eder J (2006) Soluble and cell wall-bound phenolics and lignin in Ascocalyx abietina infected Norway spruces. Plant Sci 170:563–570

    Article  Google Scholar 

  • Czyczyło-Mysza I, Tyrka M, Marcińska I, Skrzypek E, Karbarz M, Dziurka M, Hura T, Dziurka K, Quarrie SA (2013) Quantitative trait loci for leaf chlorophyll fluorescence parameters, chlorophyll and carotenoid contents in relation to biomass and yield in bread wheat and their chromosome deletion bin assignments. Mol Breed 32:189–210

    Article  PubMed  PubMed Central  Google Scholar 

  • De Ascensao ARFDC, Dubery IA (2003) Soluble and wall-bound phenolics and phenolic polymers in Musa acuminata roots exposed to elicitors from Fusarium oxysporum f.sp. cubense. Phytochemistry 63:679–686

    Article  PubMed  Google Scholar 

  • Demirbas A (2007) Progress and recent trends in biofuels. Prog Energ Combust Sci 33:1–18

    Article  CAS  Google Scholar 

  • Deverell R, McDonnell K, Ward S, Devlin G (2009) An economic assessment of potential ethanol production pathways in Ireland. Energ Policy 37:3993–4002

    Article  Google Scholar 

  • El Modafar C, El Boustani E (2001) Cell wall-bound phenolic acid and lignin contents in date palm as related to its resistance to Fusarium oxysporum. Biol Plantarum 44:125–130

    Article  Google Scholar 

  • Farber M, Attia Z, Weiss D (2016) Cytokinin activity increases stomatal density and transpiration rate in tomato. J Exp Bot. doi:10.1093/jxb/erw398

    PubMed  PubMed Central  Google Scholar 

  • Fiust A, Rapacz M, Wójcik-Jagła M, Tyrka M (2015) Development of DArT-based PCR markers for selecting drought-tolerant spring barley. J Appl Genet 56:299–309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fleury D, Jefferies S, Kuchel H, Langridge P (2010) Genetic and genomic tools to improve drought tolerance in wheat. J Exp Bot 61:3211–3222

    Article  CAS  PubMed  Google Scholar 

  • Fry SC (1982) Phenolic components of the primary cell wall. Biochem J 203:493–504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fry SC (1986) Cross-linking of matrix polymers in the growing cell walls of angiosperms. Ann Rev Plant Physiol 37:165–186

    Article  CAS  Google Scholar 

  • Fry SC (1987) Intercellular feruloylation of pectic polysaccharides. Planta 171:205–211

    Article  CAS  PubMed  Google Scholar 

  • Fu BY, Xiong JH, Zhu LH, Zhao XQ, Xu HX, Gao YM, Li YS, Xu JL, Li ZK (2007) Identification of functional candidate genes for drought tolerance in rice. Mol Gen Genomics 278:599–609

    Article  CAS  Google Scholar 

  • Giunta F, Motzo R, Deidda M (1993) Effect of drought on yield and yield components of durum wheat and triticale in a Mediterranean environment. Field Crops Res 33:399–409

    Article  Google Scholar 

  • González JM, Muñiz LM, Jouve N (2005) Mapping of QTLs for androgenetic response based on a molecular genetic map of ×Triticosecale Wittmack. Genome 48:999–1009

    Article  PubMed  Google Scholar 

  • Guan YS, Serraj R, Liu SH, Xu JL, Ali J, Wang WS, Venus E, Zhu LH, Li ZK (2010) Simultaneously improving yield under drought stress and non-stress conditions: a case study of rice (Oryza sativa L.). J Exp Bot 61:4145–4156

    Article  CAS  PubMed  Google Scholar 

  • Hackauf B, Wehling P (2002) Identification of microsatellite polymorphisms in an expressed portion of the rye genome. Plant Breeding 121:17–25

    Article  CAS  Google Scholar 

  • Hideg É, Jansen MAK, Strid Å (2013) UV-B exposure, ROS, and stress: inseparable companions or loosely linked associates? Trends Plant Sci 18:107–115

    Article  CAS  PubMed  Google Scholar 

  • Hoagland DR (1948) Lectures on the inorganic nutrition of plants. Chronica Botanica Co., Waltham, Mass. USA

  • Hura T, Grzesiak S, Hura K, Thiemt E, Tokarz K, Wedzony M (2007) Physiological and biochemical tools useful in drought tolerance detection in genotypes of winter triticale: accumulation of ferulic acid correlates with drought tolerance. Ann Bot 100:767–775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hura T, Hura K, Grzesiak S (2009a) Physiological and biochemical parameters for identification of QTLs controlling the winter triticale drought tolerance at the seedling stage. Plant Physiol Biochem 47:210–214

    Article  CAS  PubMed  Google Scholar 

  • Hura T, Hura K, Grzesiak S (2009b) Possible contribution of cell wall-bound ferulic acid in drought resistance and recovery in triticale seedlings. J Plant Physiol 166:1720–1733

    Article  CAS  PubMed  Google Scholar 

  • Hura T, Hura K, Grzesiak M (2011) Soil drought applied during the vegetative growth of triticale modifies physiological and biochemical adaptation to drought during the generative development. J Agron Crop Sci 197:113–123

    Article  Google Scholar 

  • Hura T, Hura K, Dziurka K, Ostrowska A, Bączek-Kwinta R, Grzesiak MT (2012) An increase in the content of cell wall-bound phenolics correlates with the productivity of triticale under soil drought. J Plant Physiol 169:1728–1736

    Article  CAS  PubMed  Google Scholar 

  • Hura T, Hura K, Ostrowska A, Grzesiak M, Dziurka K (2013) The cell wall-bound phenolics as a biochemical indicator of soil drought resistance in winter triticale. Plant Soil Environ 59:189–195

    Article  CAS  Google Scholar 

  • Hura K, Hura T, Dziurka K, Dziurka M (2015) Carbohydrate, phenolic and antioxidant level in relation to chlorophyll a content in oilseed winter rape (Brassica napus L.) inoculated with Leptosphaeria maculans. Eur J Plant Pathol 143:291–303

    Article  CAS  Google Scholar 

  • Hura T, Dziurka M, Hura K, Ostrowska A, Dziurka K (2016) Different allocation of carbohydrates and phenolics in dehydrated leaves of triticale. J Plant Physiol 202:1–9

    Article  CAS  PubMed  Google Scholar 

  • Jordan WR, Dugas WA Jr, Shouse PJ (1983) Strategies for crop improvement for drought-prone regions. Agric Water Manag 7:281–299

    Article  Google Scholar 

  • Jorgensen JR, Deleuran LC, Wollenweber B (2007) Prospects of whole grain crops of wheat, rye and triticale under different fertilizer regimes for energy production. Biomass Bioenerg 31:308–317

    Article  Google Scholar 

  • Kamisaka S, Takeda S, Takahashi K, Shibata K (1990) Diferulic and ferulic acid in the cell wall of Avena coleoptiles: their relationships to mechanical properties of the cell wall. Physiol Plant 78:1–7

    Article  CAS  Google Scholar 

  • Kumar A, Berier J, Verulkar S, Lafitte HR, Atlin GN (2008) Breeding for drought tolerance: direct selection for yield, response to selection and use of drought-tolerant donors in upland and lowland-adapted populations. Field Crops Res 107:221–231

    Article  Google Scholar 

  • Lichtenthaler HK, Schweiger J (1998) Cell wall bound ferulic acid, the major substance of the blue-green fluorescence emission of plants. J Plant Physiol 152:272–282

    Article  CAS  Google Scholar 

  • Lin CC, Kao CH (2001) Cell wall peroxidase activity, hydrogen peroxide level and NaCl-inhibited root growth of rice seedlings. Plant Soil 230:135–143

    Article  CAS  Google Scholar 

  • Lopes MS, Araus JL, van Heerden PDR, Foyer CH (2011) Enhancing drought tolerance in C4 crops. J Exp Bot 62:3135–3153

    Article  CAS  PubMed  Google Scholar 

  • Lorenz K, Pomeranz Y (1974) The history, development, and utilization of triticale. CRC Crit Rev Food Technol 5:175–280

    Article  Google Scholar 

  • Macková H, Hronková M, Dobrá J, Turečková V, Novák O, Lubovská Z, Motyka V, Haisel D, Hájek T, Prášil IT, Gaudinová A, Štorchová H, Ge E, Werner T, Schmülling T, Vanková R (2013) Enhanced drought and heat stress tolerance of tobacco plants with ectopically enhanced cytokinin oxidase/dehydrogenase gene expression. J Exp Bot 64:2805–2815

    Article  PubMed  PubMed Central  Google Scholar 

  • Mahmud I, Kramer HI (1951) Segregation for yield, height, and maturity following a soybean cross. Agron J 43:605–609

    Article  Google Scholar 

  • Mandal S, Mitra A, Mallick N (2009) Time course study on accumulation of cell wall-bound phenolics and activities of defense enzymes in tomato roots in relation to Fusarium wilt. World J Microbiol Biotech 25:795–802

    Article  CAS  Google Scholar 

  • Marino R, Ponnaiah M, Krajewski P, Frova C, Gianfranceschi L, Pe EM, Gorla SM (2009) Addressing drought tolerance in maize by transcriptional profiling and mapping. Mol Genet Genomics 218:163–179

    Article  Google Scholar 

  • Martorell S, Diaz-Espejo A, Medrano H, Ball MC, Choat B (2014) Rapid hydraulic recovery in Eucalyptus pauciflora after drought: linkages between stem hydraulics and leaf gas exchange. Plant Cell Environ 37:617–626

    Article  CAS  PubMed  Google Scholar 

  • Nguyen TT, Klueva N, Chamareck V, Aarti A, Magpantay G, Millena AC, Pathan MS, Nguyen HT (2004) Saturation mapping of QTL regions and identification of putative candidate genes for drought tolerance in rice. Mol Genet Genomics 272:35–46

    Article  CAS  PubMed  Google Scholar 

  • Nishiyama R, Watanabe Y, Fujita Y, Le DT, Kojima M, Werner T, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Kakimoto T, Sakakibara H, Schmülling T, Tran LS (2011) Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 23:2169–2183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nogués S, Baker NR (2000) Effects of drought on photosynthesis in Mediterranean plants grown under enhanced UV-B radiation. J Exp Bot 51:1309–1317

    PubMed  Google Scholar 

  • Nogués S, Allen DJ, Morison JIL, Baker NR (1998) Ultraviolet-B radiation effects on water relations, leaf development, and photosynthesis in droughted pea plants. Plant Physiol 117:173–181

    Article  PubMed  PubMed Central  Google Scholar 

  • Pastenes C, Pimentel P, Lillo J (2005) Leaf movements and photoinhibition in relation to water stress in field-grown beans. J Exp Bot 56:425–433

    Article  CAS  PubMed  Google Scholar 

  • Pejin D, Mojovic LJ, Vucurovic V, Pejin J, Dencic S, Rakin M (2009) Fermentation of wheat and triticale hydrolysates: a comparative study. Fuel 88:1625–1628

    Article  CAS  Google Scholar 

  • Pestsova E, Ganal MW, Röder MS (2000) Isolation and mapping of microsatellite markers specific for the D genome of bread wheat. Genome 43:689–697

    Article  CAS  PubMed  Google Scholar 

  • Röder MS, Korzun V, Wendehake K, Plaschke J, Tixier MH, Leroy P, Ganal MW (1998) A microsatellite map of wheat. Genetics 149:2007–2023

    PubMed  PubMed Central  Google Scholar 

  • Rodriguez-Iturbe I (2000) Ecohydrology: a hydrologic perspective of climate-soil-vegetation dynamics. Water Resour Res 36:3–9

    Article  Google Scholar 

  • Rosenberger A, Kaul HP, Senn T, Aufhammer W (2002) Costs of bioethanol production from winter cereals: the effect of growing conditions and crop production intensity levels. Ind Crops Prod 15:91–102

    Article  CAS  Google Scholar 

  • Saal B, Wricke G (1999) Development of simple sequence repeat markers in rye (Secale cereale L.). Genome 42:964–972

    Article  CAS  PubMed  Google Scholar 

  • Salvi S, Tuberosa R (2005) To clone or not to clone plant QTLs: present and future challenges. Trends Plant Sci 10:297–304

    Article  CAS  PubMed  Google Scholar 

  • Santiago R, de Armas R, Fontaniella B, Vicente C, Legaz ME (2009) Changes in soluble and cell wall-bound hydroxycinnamic and hydroxybenzoic acids in sugarcane cultivars inoculated with Sporisorium scitamineum sporidia. Eur J Plant Pathol 124:439–450

    Article  CAS  Google Scholar 

  • Schopfer P (1996) Hydrogen peroxide-mediated cell-wall stiffening in vitro in maize coleoptiles. Planta 199:43–49

    Article  CAS  Google Scholar 

  • Schweiger J, Lang M, Lichtenthaler HK (1996) Differences in fluorescence excitation spectra of leaves between stressed and non-stressed plants. J Plant Physiol 148:536–547

    Article  CAS  Google Scholar 

  • Singleton VS, Rossi JA Jr (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagent. Am J Enol Vitic 16:144–157

    CAS  Google Scholar 

  • Solomon BD (2010) Biofuels and sustainability. Ann NY Acad Sci 1185:119–134

    Article  PubMed  Google Scholar 

  • Somers DJ, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109:1105–1114

    Article  CAS  PubMed  Google Scholar 

  • Strasser RJ, Tsimilli-Michael M (2001) Stress in plants, from daily rhythm to global changes, detected and quantified by the JIP–Test. Chim Nouvelle 75:3321–3326

    Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V (2010) Simultaneous in vivo recording of prompt and delayed fluorescence and 820 nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochim Biophys Acta 1797:1313–1326

    Article  CAS  PubMed  Google Scholar 

  • Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16:53–60

    Article  CAS  PubMed  Google Scholar 

  • Talbott LD, Zeiger E (1998) The role of sucrose in guard cell osmoregulation. J Exp Bot 49:329–337

    Article  Google Scholar 

  • Tsimilli-Michael M, Strasser RJ (2008) In vivo assessment of plant’s vitality: applications in detecting and evaluating the impact of mycorrhization on host plants. In: Varma A (ed) Mycorrhiza, State of the Art, Genetics, and Molecular Biology, Eco-Function, Biotechnology, Eco-Physiology, Structure, and Systematics, 3rd edn. Springer, Dordrecht, The Netherlands, pp. 679–703

  • Turner NC, Blum A, Cakir M, Steduto P, Tuberosa R, Young N (2014) Strategies to increase the yield and yield stability of crops under drought—are we making progress? Funct Plant Biol 41:1199–1206

    Article  Google Scholar 

  • Tyrka M, Bednarek PT, Kilian A, Wędzony M, Hura T, Bauer E (2011) Genetic map of triticale compiling DArT, SSR, and AFLP markers. Genome 54:391–401

    Article  CAS  PubMed  Google Scholar 

  • Tyrka M, Tyrka D, Wędzony M (2015) Genetic map of triticale integrating microsatellite. DArT and SNP markers. PLoS One 10:e0145714

    Article  PubMed  PubMed Central  Google Scholar 

  • van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150

    Article  PubMed  Google Scholar 

  • van Ooijen JW (2006) JoinMap ® 4. Software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen, Netherlands (online)

  • van Os H, Stam P, Visser RGF, van Eck HJ (2005) RECORD: a novel method for ordering loci on a genetic linkage map. Theor Appl Genet 112:30–40

    Article  CAS  PubMed  Google Scholar 

  • Wakabayashi K, Hoson T, Kamisaka S (1997) Osmotic stress suppresses cell wall stiffening and the increase in cell wall-bound ferulic and diferulic acids in wheat coleoptiles. Plant Physiol 113:967–973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, Basten CJ, Zeng ZB (2012) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh

  • Wang J, Li H, Zhang L, Meng L (2014) Users’ manual of QTL IciMapping. The Quantitative Genetics Group, Institute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100081, China, and Genetic Resources Program, International Maize and Wheat Improvement Center (CIMMYT), Apdo. Postal 6-641, 06600 Mexico, D.F., Mexico

  • Wędzony M (2003) Protocol for anther culture in hexaploid triticale (×Triticosecale Wittm.). In: Małuszynski M et al (eds) Doubled haploid production in crop plants. A manual. Kluwer Academic Publisher, Dordrecht, pp 123–128

  • Werner T, Nehnevajovaa E, Köllmera I, Novákb O, Strnadb M, Krämerc U, Schmüllinga T (2010) Root-specific reduction of cytokinin causes enhanced root growth, drought tolerance, and leaf mineral enrichment in Arabidopsis and tobacco. Plant Cell 22:3905–3920

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tomasz Hura.

Ethics declarations

Funding

The study was supported by the National Centre for Research and Development (Poland), Project GENMARK (PBS1/A8/1/2012; PBS1 177 150).

Conflict of interest

All authors have no conflicts of interest to declare.

Ethical standards

This article does not describe any studies with human participants or animals performed by any of the authors.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

Below is the link to the electronic supplementary material.

438_2016_1276_MOESM1_ESM.xlsx

Appendix S1. QTL_source_sequences: Sequences of DArTseq markers and DArT clones for 5 QTLs influencing cell wall phenolic compounds content in triticale mapping population of Hewo x Magnat. (XLSX 20 kb)

438_2016_1276_MOESM2_ESM.xlsx

Appendix S2. URGI-Contigs: Contigs identified after BLASTing of DArTseq markers (from regions of QCWPh) vs. wheat genome deposited at URGI database. (XLSX 14 kb)

438_2016_1276_MOESM3_ESM.xlsx

Appendix S3. NCBI-BLAST: Complete list of genes from NCBI database matching contig sequences corresponding to regions affecting CWPh. (XLSX 21 kb)

438_2016_1276_MOESM4_ESM.jpg

Figure S1. A two-dimensional plot based on a principal coordinate analysis of phenotypic variation in Hewo x Magnat mapping population at the vegetative stage (V). (JPEG 382 kb)

438_2016_1276_MOESM5_ESM.jpg

Figure S2. A two-dimensional plot based on a principal coordinate analysis of phenotypic variation in Hewo x Magnat mapping population at the generative stage (G). (JPEG 411 kb)

438_2016_1276_MOESM6_ESM.docx

Table S1. Summary statistics for all studied traits of the two parental lines and their DH lines at the vegetative (V) and generative (G) developmental stages of triticale growth. (DOCX 15 kb)

438_2016_1276_MOESM7_ESM.docx

Table S2. Coefficients and eigenvalues for the first 6 principal components based on Pearson correlation matrix between traits at the vegetative stage (V). (DOCX 17 kb)

438_2016_1276_MOESM8_ESM.docx

Table S3. Coefficients and eigenvalues for the first 6 principal components based on Pearson correlation matrix between traits at the generative stage (G). (DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hura, T., Tyrka, M., Hura, K. et al. QTLs for cell wall-bound phenolics in relation to the photosynthetic apparatus activity and leaf water status under drought stress at different growth stages of triticale. Mol Genet Genomics 292, 415–433 (2017). https://doi.org/10.1007/s00438-016-1276-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-016-1276-y

Keywords

Navigation