Assessment of synthetic hexaploid wheats in response to heat stress and leaf rust infection for the improvement of wheat production
Hai An Truong A , Won Je Lee A , Masahiro Kishii B , Suk-Whan Hong C , Chon-Sik Kang D , Byung Cheon Lee A and Hojoung Lee
A E
+ Author Affiliations
- Author Affiliations
A Department of Biosystems and Biotechnology, College of Life Sciences and Biotechnology, Korea University, Anam-dong 5-ga, Seongbuk-gu, Seoul 02841, Republic of Korea.
B Global Wheat Program, International Maize and Wheat Improvement Center, Carretera México-Veracruz Km. 45, El Batán, Texcoco, México, C.P. 56237.
C Department of Molecular Biotechnology, College of Agriculture and Life Sciences, Bioenergy Research Center, Chonnam National University, Gwangju 61186, Republic of Korea.
D Crop Breeding Division, National Institute of Crop Science, Rural Development Administration, Wanju 55365, Republic of Korea.
E Corresponding author. Email: lhojoung@korea.ac.kr
Crop and Pasture Science 70(10) 837-848 https://doi.org/10.1071/CP19111
Submitted: 18 March 2019 Accepted: 2 September 2019 Published: 29 October 2019
Abstract
Bread wheat (Triticum aestivum L.) is a popular cereal crop worldwide, but its future use is threatened by its limited genetic diversity because of the evolutionary bottleneck limiting its ability to combat abiotic and biotic stresses. However, synthetic hexaploid wheat (SHW) is known for its genetic diversity resulting from of the artificial crossing used to transfer elite genes from donors. SHW is therefore a potential source for genetic variations to combat stress. We studied two SHW lines from CYMMIT (cSHW339464 and cSHW339465) and a Korean bread wheat (cv. KeumKang) to determine their ability to tolerate heat stress and leaf rust infection. Our results showed that cSHW339464 could tolerate heat stress because of its maintained-green phenotype, high accumulation of anthocyanin, antioxidant activity (DPPH), proline content, and the response of heat-shock proteins after being challenged by heat stress. On the other hand, cSHW339465 is resistant to leaf rust and can inhibit the growth of pathogens on the leaf surface, owing to the induction of genes encoding β-1,3-glucanase and peroxidase and subsequent enzyme activities. In conclusion, these two SHW lines could prove good candidates contributing to the improvement of current wheat resources.
Additional keywords: anthocyanin, bread wheat, breading material, peroxidase.
References
Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010) Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Critical Reviews in Biotechnology 30, 161–175.| Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress.Crossref | GoogleScholarGoogle Scholar | 20214435PubMed |
Anguelova-Merhar VS, van der Westhuizen AJ, Pretorius ZA (2002) Intercellular chitinase and peroxidase activities associated with resistance conferred by gene Lr35 to leaf rust of wheat. Journal of Plant Physiology 159, 1259–1261.
| Intercellular chitinase and peroxidase activities associated with resistance conferred by gene Lr35 to leaf rust of wheat.Crossref | GoogleScholarGoogle Scholar |
Ayliffe M, Periyannan SK, Feechan A, Dry I, Schumann U, Wang M-B, Pryor A, Lagudah E (2013) A simple method for comparing fungal biomass in infected plant tissues. Molecular Plant-Microbe Interactions 26, 658–667.
| A simple method for comparing fungal biomass in infected plant tissues.Crossref | GoogleScholarGoogle Scholar | 23405866PubMed |
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry 44, 276–287.
| Superoxide dismutase: improved assays and an assay applicable to acrylamide gels.Crossref | GoogleScholarGoogle Scholar | 4943714PubMed |
Benhamou N, Joosten MHAJ, Wit PJGMD (1990) Subcellular localization of chitinase and of its potential substrate in tomato root tissues infected by Fusarium oxysporum f. sp. radicis-lycopersici. Plant Physiology 92, 1108–1120.
| Subcellular localization of chitinase and of its potential substrate in tomato root tissues infected by Fusarium oxysporum f. sp. radicis-lycopersici.Crossref | GoogleScholarGoogle Scholar | 16667378PubMed |
Bhatta M, Regassa T, Rose DJ, Baenziger PS, Eskridge KM, Santra DK, Poudel R (2017) Genotype, environment, seeding rate, and top-dressed nitrogen effects on end-use quality of modern Nebraska winter wheat. Journal of the Science of Food and Agriculture 97, 5311–5318.
| Genotype, environment, seeding rate, and top-dressed nitrogen effects on end-use quality of modern Nebraska winter wheat.Crossref | GoogleScholarGoogle Scholar | 28485012PubMed |
Blättel V, Larisika M, Pfeiffer P, Nowak C, Eich A, Eckelt J, König H (2011) Beta-1,3-glucanase from Delftia tsuruhatensis strain MV01 and its potential application in vinification. Applied and Environmental Microbiology 77, 983–990.
| Beta-1,3-glucanase from Delftia tsuruhatensis strain MV01 and its potential application in vinification.Crossref | GoogleScholarGoogle Scholar | 21169426PubMed |
Bolton MD, Kolmer JA, Garvin DF (2008) Wheat leaf rust caused by Puccinia triticina. Molecular Plant Pathology 9, 563–575.
| Wheat leaf rust caused by Puccinia triticina.Crossref | GoogleScholarGoogle Scholar | 19018988PubMed |
Bonjean AP, Angus WJ (Eds) (2001) ‘The world wheat book: a history of wheat breeding.’ (Lavoisier: Paris)
Börner A, Ogbonnaya FC, Röder MS, Rasheed A, Periyannan S, Lagudah ES (2015) Aegilops tauschii introgressions in wheat. In ‘Alien introgression in wheat: cytogenetics, molecular biology, and genomics’. (Eds M Molnár-Láng, C Ceoloni, J Doležel) pp. 245–271. (Springer International Publishing: Cham, Switzerland)
Casey LW, Lavrencic P, Bentham AR, Cesari S, Ericsson DJ, Croll T, Turk D, Anderson PA, Mark AE, Dodds PN, Mobli M, Kobe B, Williams SJ (2016) The CC domain structure from the wheat stem rust resistance protein Sr33 challenges paradigms for dimerization in plant NLR proteins. Proceedings of the National Academy of Sciences of the United States of America 113, 12856–12861.
| The CC domain structure from the wheat stem rust resistance protein Sr33 challenges paradigms for dimerization in plant NLR proteins.Crossref | GoogleScholarGoogle Scholar |
Castellarin SD, Pfeiffer A, Sivilotti P, Degan M, Peterlunger EDI, Gaspero G (2007) Transcriptional regulation of anthocyanin biosynthesis in ripening fruits of grapevine under seasonal water deficit. Plant, Cell & Environment 30, 1381–1399.
| Transcriptional regulation of anthocyanin biosynthesis in ripening fruits of grapevine under seasonal water deficit.Crossref | GoogleScholarGoogle Scholar |
Cawood ME, Pretorius JC, van der Westhuizen AJ, Pretorius ZA (2010) Disease development and PR-protein activity in wheat (Triticum aestivum) seedlings treated with plant extracts prior to leaf rust (Puccinia triticina) infection. Crop Protection 29, 1311–1319.
| Disease development and PR-protein activity in wheat (Triticum aestivum) seedlings treated with plant extracts prior to leaf rust (Puccinia triticina) infection.Crossref | GoogleScholarGoogle Scholar |
Chauhan H, Khurana N, Nijhavan A, Khurana JP, Khurana P (2012) The wheat chloroplastic small heat shock protein (sHSP26) is involved in seed maturation and germination and imparts tolerance to heat stress. Plant, Cell & Environment 35, 1912–1931.
| The wheat chloroplastic small heat shock protein (sHSP26) is involved in seed maturation and germination and imparts tolerance to heat stress.Crossref | GoogleScholarGoogle Scholar |
Choi S, Seo H-S, Lee KR, Lee S, Lee J (2018) Effect of cultivars and milling degrees on free and bound phenolic profiles and antioxidant activity of black rice. Applied Biological Chemistry 61, 49–60.
| Effect of cultivars and milling degrees on free and bound phenolic profiles and antioxidant activity of black rice.Crossref | GoogleScholarGoogle Scholar |
Chu C-G, Friesen TL, Xu SS, Faris JD, Kolmer JA (2009) Identification of novel QTLs for seedling and adult plant leaf rust resistance in a wheat doubled haploid population. Theoretical and Applied Genetics 119, 263–269.
| Identification of novel QTLs for seedling and adult plant leaf rust resistance in a wheat doubled haploid population.Crossref | GoogleScholarGoogle Scholar | 19396420PubMed |
Cossani CM, Reynolds MP (2015) Heat stress adaptation in elite lines derived from synthetic hexaploid wheat. Crop Science 55, 2719–2735.
| Heat stress adaptation in elite lines derived from synthetic hexaploid wheat.Crossref | GoogleScholarGoogle Scholar |
Das MK, Bai G, Mujeeb-Kazi A, Rajaram S (2016) Genetic diversity among synthetic hexaploid wheat accessions (Triticum aestivum) with resistance to several fungal diseases. Genetic Resources and Crop Evolution 63, 1285–1296.
| Genetic diversity among synthetic hexaploid wheat accessions (Triticum aestivum) with resistance to several fungal diseases.Crossref | GoogleScholarGoogle Scholar |
de Leonardis AM, Fragasso M, Beleggia R, Ficco DBM, de Vita P, Mastrangelo AM (2015) Effects of heat stress on metabolite accumulation and composition, and nutritional properties of durum wheat grain. International Journal of Molecular Sciences 16, 30382–30404.
| Effects of heat stress on metabolite accumulation and composition, and nutritional properties of durum wheat grain.Crossref | GoogleScholarGoogle Scholar | 26703576PubMed |
Ficco DBM, De Simone V, Colecchia SA, Pecorella I, Platani C, Nigro F, Finocchiaro F, Papa R, De Vita P (2014) Genetic variability in anthocyanin composition and nutritional properties of blue, purple, and red bread (Triticum aestivum L.) and durum (Triticum turgidum L. ssp. turgidum convar. durum) wheats. Journal of Agricultural and Food Chemistry 62, 8686–8695.
| Genetic variability in anthocyanin composition and nutritional properties of blue, purple, and red bread (Triticum aestivum L.) and durum (Triticum turgidum L. ssp. turgidum convar. durum) wheats.Crossref | GoogleScholarGoogle Scholar |
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.
| Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants.Crossref | GoogleScholarGoogle Scholar | 20870416PubMed |
Grassini P, Eskridge KM, Cassman KG (2013) Distinguishing between yield advances and yield plateaus in historical crop production trends. Nature Communications 4, 2918
Huerta-Espino J, Singh RP, Germán S, McCallum BD, Park RF, Chen WQ, Bhardwaj SC, Goyeau H (2011) Global status of wheat leaf rust caused by Puccinia triticina. Euphytica 179, 143–160.
| Global status of wheat leaf rust caused by Puccinia triticina.Crossref | GoogleScholarGoogle Scholar |
Jafarzadeh J, Bonnett D, Jannink J-L, Akdemir D, Dreisigacker S, Sorrells ME (2016) Breeding Value of primary synthetic wheat genotypes for grain yield. PLoS One 11, e0162860
| Breeding Value of primary synthetic wheat genotypes for grain yield.Crossref | GoogleScholarGoogle Scholar | 27656893PubMed |
Jeong CY, Lee WJ, Truong HA, Trịnh CS, Hong S-W, Lee H (2018) AtMybL-O modulates abscisic acid biosynthesis to optimize plant growth and ABA signaling in response to drought stress. Applied Biological Chemistry 61, 473–477.
| AtMybL-O modulates abscisic acid biosynthesis to optimize plant growth and ABA signaling in response to drought stress.Crossref | GoogleScholarGoogle Scholar |
Jighly A, Alagu M, Makdis F, Singh M, Singh S, Emebiri LC, Ogbonnaya FC (2016) Genomic regions conferring resistance to multiple fungal pathogens in synthetic hexaploid wheat. Molecular Breeding 36, 127
| Genomic regions conferring resistance to multiple fungal pathogens in synthetic hexaploid wheat.Crossref | GoogleScholarGoogle Scholar |
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
| Proline induces heat tolerance in chickpea (Cicer arietinum L.) plants by protecting vital enzymes of carbon and antioxidative metabolism.Crossref | GoogleScholarGoogle Scholar | 23573011PubMed |
Kirubakaran SI, Sakthivel N (2007) Cloning and overexpression of antifungal barley chitinase gene in Escherichia coli. Protein Expression and Purification 52, 159–166.
| Cloning and overexpression of antifungal barley chitinase gene in Escherichia coli.Crossref | GoogleScholarGoogle Scholar | 17029984PubMed |
Kobayashi F, Ishibashi M, Takumi S (2008) Transcriptional activation of Cor/Lea genes and increase in abiotic stress tolerance through expression of a wheat DREB2 homolog in transgenic tobacco. Transgenic Research 17, 755–767.
| Transcriptional activation of Cor/Lea genes and increase in abiotic stress tolerance through expression of a wheat DREB2 homolog in transgenic tobacco.Crossref | GoogleScholarGoogle Scholar | 18034365PubMed |
Lage J, Warburton ML, Crossa J, Skovmand B, Andersen SB (2003) Assessment of genetic diversity in synthetic hexaploid wheats and their Triticum dicoccum and Aegilops tauschii parents using AFLPs and agronomic traits. Euphytica 134, 305–317.
| Assessment of genetic diversity in synthetic hexaploid wheats and their Triticum dicoccum and Aegilops tauschii parents using AFLPs and agronomic traits.Crossref | GoogleScholarGoogle Scholar |
Lee JM, Tan WS, Ting ASY (2014) Revealing the antimicrobial and enzymatic potentials of culturable fungal endophytes from tropical pitcher plants (Nepenthes spp.). Mycosphere 5, 364–377.
| Revealing the antimicrobial and enzymatic potentials of culturable fungal endophytes from tropical pitcher plants (Nepenthes spp.).Crossref | GoogleScholarGoogle Scholar |
Lee H, Hwang MH, Cho M, Lee DG, Go EB, Cheong Y-K, Kang C-S, Lee NT, Chung N (2017a) Comparison of blood glucose levels and allergic responses on treatment with six wheat cultivars. Applied Biological Chemistry 60, 11–16.
| Comparison of blood glucose levels and allergic responses on treatment with six wheat cultivars.Crossref | GoogleScholarGoogle Scholar |
Lee WJ, Kim J, Lee D, Hong SW, Lee H (2017b) Arabidopsis UDP-glycosyltransferase 78D1-overexpressing plants accumulate higher levels of kaempferol 3-O-β-d-glucopyranoside than wild-type plants. Applied Biological Chemistry 60, 647–652.
| Arabidopsis UDP-glycosyltransferase 78D1-overexpressing plants accumulate higher levels of kaempferol 3-O-β-d-glucopyranoside than wild-type plants.Crossref | GoogleScholarGoogle Scholar |
Li J, Wan H-S, Yang W-Y (2014) Synthetic hexaploid wheat enhances variation and adaptive evolution of bread wheat in breeding processes. Journal of Systematics and Evolution 52, 735–742.
| Synthetic hexaploid wheat enhances variation and adaptive evolution of bread wheat in breeding processes.Crossref | GoogleScholarGoogle Scholar |
Li A, Liu D, Yang W, Kishii M, Mao L (2018) Synthetic hexaploid wheat: yesterday, today, and tomorrow. Engineering 4, 552–558.
| Synthetic hexaploid wheat: yesterday, today, and tomorrow.Crossref | GoogleScholarGoogle Scholar |
Liao F, Pan R (2001) Accumulation of proline under heat-stress and function on heat-tolerance in Brassica campestris L. SSP. chinesis var. utilis tsen et Lee. Journal of South China Normal University (Natural Science) 2, 45–49.
Lindquist S (1986) The heat-shock response. Annual Review of Biochemistry 55, 1151–1191.
| The heat-shock response.Crossref | GoogleScholarGoogle Scholar | 2427013PubMed |
Lindquist S, Craig EA (1988) The heat-shock proteins. Annual Review of Genetics 22, 631–677.
| The heat-shock proteins.Crossref | GoogleScholarGoogle Scholar | 2853609PubMed |
Liu B, Asseng S, Müller C, Ewert F, Elliott J, Lobell DB, Martre P, Ruane AC, Wallach D, Jones JW, Rosenzweig C, Aggarwal PK, Alderman PD, Anothai J, Basso B, Biernath C, Cammarano D, Challinor A, Deryng D, Sanctis GD, Doltra J, Fereres E, Folberth C, Garcia-Vila M, Gayler S, Hoogenboom G, Hunt LA, Izaurralde RC, Jabloun M, Jones CD, Kersebaum KC, Kimball BA, Koehler AK, Kumar SN, Nendel C, O’Leary GJ, Olesen JE, Ottman MJ, Palosuo T, Prasad PVV, Priesack E, Pugh TAM, Reynolds M, Rezaei EE, Rötter RP, Schmid E, Semenov MA, Shcherbak I, Stehfest E, Stöckle CO, Stratonovitch P, Streck T, Supit I, Tao F, Thorburn P, Waha K, Wall GW, Wang E, White JW, Wolf J, Zhao Z, Zhu Y (2016) Similar estimates of temperature impacts on global wheat yield by three independent methods. Nature Climate Change 6, 1130–1136.
| Similar estimates of temperature impacts on global wheat yield by three independent methods.Crossref | GoogleScholarGoogle Scholar |
Majka M, Kwiatek MT, Majka J, Wiśniewska H (2017) Aegilops tauschii accessions with geographically diverse origin show differences in chromosome organization and polymorphism of molecular markers linked to leaf rust and powdery mildew resistance genes. Frontiers in Plant Science 8, 1149
| Aegilops tauschii accessions with geographically diverse origin show differences in chromosome organization and polymorphism of molecular markers linked to leaf rust and powdery mildew resistance genes.Crossref | GoogleScholarGoogle Scholar | 28702048PubMed |
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Analytical Chemistry 31, 426–428.
| Use of dinitrosalicylic acid reagent for determination of reducing sugar.Crossref | GoogleScholarGoogle Scholar |
Muench-Garthoff S, Neuhaus J-M, Boller T, Kemmerling B, Kogel K-H (1997) Expression of beta-1,3-glucanase and chitinase in healthy, stem-rust-affected and elicitor-treated near-isogenic wheat lines showing Sr5-or Sr24-specified race-specific rust resistance. Planta 201, 235–244.
Mujeeb-Kazi A, Rosas V, Roldan S (1996) Conservation of the genetic variation of Triticum tauschii (Coss.) Schmalh. (Aegilops squarrosa auct. non L.) in synthetic hexaploid wheats (T. turgidum L. s.lat. x T. tauschii; 2n=6x=42, AABBDD) and its potential utilization for wheat improvement. Genetic Resources and Crop Evolution 43, 129–134.
| Conservation of the genetic variation of Triticum tauschii (Coss.) Schmalh. (Aegilops squarrosa auct. non L.) in synthetic hexaploid wheats (T. turgidum L. s.lat. x T. tauschii; 2n=6x=42, AABBDD) and its potential utilization for wheat improvement.Crossref | GoogleScholarGoogle Scholar |
Naz AA, Kunert A, Lind V, Pillen K, Léon J (2008) AB-QTL analysis in winter wheat: II. Genetic analysis of seedling and field resistance against leaf rust in a wheat advanced backcross population. Theoretical and Applied Genetics 116, 1095–1104.
| AB-QTL analysis in winter wheat: II. Genetic analysis of seedling and field resistance against leaf rust in a wheat advanced backcross population.Crossref | GoogleScholarGoogle Scholar | 18338154PubMed |
Ogbonnaya FC, Imtiaz M, Bariana HS, McLean M, Shankar MM, Hollaway GJ, Trethowan RM, Lagudah ES, van Ginkel M (2008) Mining synthetic hexaploids for multiple disease resistance to improve bread wheat. Australian Journal of Agricultural Research 59, 421–431.
| Mining synthetic hexaploids for multiple disease resistance to improve bread wheat.Crossref | GoogleScholarGoogle Scholar |
Park C-J, Seo Y-S (2015) Heat shock proteins: a review of the molecular chaperones for plant immunity. The Plant Pathology Journal 31, 323–333.
| Heat shock proteins: a review of the molecular chaperones for plant immunity.Crossref | GoogleScholarGoogle Scholar | 26676169PubMed |
Pinto da Silva GB, Zanella CM, Martinelli JA, Chaves MS, Hiebert CW, McCallum BD, Boyd LA (2018) Quantitative trait loci conferring leaf rust resistance in hexaploid wheat. Phytopathology 108, 1344–1354.
| Quantitative trait loci conferring leaf rust resistance in hexaploid wheat.Crossref | GoogleScholarGoogle Scholar | 30211634PubMed |
Rafique K, Rauf CA, Gul A, Bux H, Memon RA, Ali A, Farrakh S (2017) Evaluation of d-genome synthetic hexaploid wheats and advanced derivatives for powdery mildew resistance. Pakistan Journal of Botany 49, 735–743.
Schnippenkoetter W, Lo C, Liu G, Dibley K, Chan WL, White J, Milne R, Zwart A, Kwong E, Keller B, Godwin I, Krattinger SG, Lagudah E (2017) The wheat Lr34 multipathogen resistance gene confers resistance to anthracnose and rust in sorghum. Plant Biotechnology Journal 15, 1387–1396.
| The wheat Lr34 multipathogen resistance gene confers resistance to anthracnose and rust in sorghum.Crossref | GoogleScholarGoogle Scholar | 28301718PubMed |
Seevers PM, Daly JM, Catedral FF (1971) The role of peroxidase isozymes in resistance to wheat stem rust disease 1. Plant Physiology 48, 353–360.
| The role of peroxidase isozymes in resistance to wheat stem rust disease 1.Crossref | GoogleScholarGoogle Scholar | 16657797PubMed |
Song K, Yim WC, Lee B-M (2017) Expression of heat shock proteins by heat stress in soybean. Plant Breeding and Biotechnology 5, 344–353.
| Expression of heat shock proteins by heat stress in soybean.Crossref | GoogleScholarGoogle Scholar |
Truong HA, Jeong CY, Lee WJ, Lee BC, Chung N, Kang C-S, Cheong Y-K, Hong S-W, Lee H (2017) Evaluation of a rapid method for screening heat stress tolerance using three Korean wheat (Triticum aestivum L.) cultivars. Journal of Agricultural and Food Chemistry 65, 5589–5597.
| Evaluation of a rapid method for screening heat stress tolerance using three Korean wheat (Triticum aestivum L.) cultivars.Crossref | GoogleScholarGoogle Scholar | 28650654PubMed |
Türkan I, Demiral T (2009) Recent developments in understanding salinity tolerance. Environmental and Experimental Botany 67, 2–9.
| Recent developments in understanding salinity tolerance.Crossref | GoogleScholarGoogle Scholar |
Usman MG, Rafii MY, Ismail MR, Malek MA, Latif MA (2015) Expression of target gene Hsp70 and membrane stability determine heat tolerance in chili pepper. Journal of the American Society for Horticultural Science 140, 144–150.
| Expression of target gene Hsp70 and membrane stability determine heat tolerance in chili pepper.Crossref | GoogleScholarGoogle Scholar |
van Ginkel M, Ogbonnaya F (2007) Novel genetic diversity from synthetic wheats in breeding cultivars for changing production conditions. Field Crops Research 104, 86–94.
| Novel genetic diversity from synthetic wheats in breeding cultivars for changing production conditions.Crossref | GoogleScholarGoogle Scholar |
Yang H, Shin Y (2017) Antioxidant compounds and activities of edible roses (Rosa hybrida spp.) from different cultivars grown in Korea. Applied Biological Chemistry 60, 129–136.
| Antioxidant compounds and activities of edible roses (Rosa hybrida spp.) from different cultivars grown in Korea.Crossref | GoogleScholarGoogle Scholar |
Yang W, Liu D, Li J, Zhang L, Wei H, Hu X, Zheng Y, He Z, Zou Y (2009) Synthetic hexaploid wheat and its utilization for wheat genetic improvement in China. Journal of Genetics and Genomics 36, 539–546.
| Synthetic hexaploid wheat and its utilization for wheat genetic improvement in China.Crossref | GoogleScholarGoogle Scholar | 19782955PubMed |
Yüzbaşioğlu E, Dalyan E, Akpinar I (2017) Changes in photosynthetic pigments, anthocyanin content and antioxidant enzyme activities of maize (Zea mays L.) seedlings under high temperature stress conditions. Trakya University Journal of Natural Science 18, 97–104.
| Changes in photosynthetic pigments, anthocyanin content and antioxidant enzyme activities of maize (Zea mays L.) seedlings under high temperature stress conditions.Crossref | GoogleScholarGoogle Scholar |
Zhang P, Dreisigacker S, Melchinger AE, Reif JC, Kazi AM, Van Ginkel M, Hoisington D, Warburton ML (2005) Quantifying novel sequence variation and selective advantage in synthetic hexaploid wheats and their backcross-derived lines using SSR markers. Molecular Breeding 15, 1–10.
| Quantifying novel sequence variation and selective advantage in synthetic hexaploid wheats and their backcross-derived lines using SSR markers.Crossref | GoogleScholarGoogle Scholar |
Zhang J, Wang F, Liang F, Zhang Y, Ma L, Wang H, Liu D (2018) Functional analysis of a pathogenesis-related thaumatin-like protein gene TaLr35PR5 from wheat induced by leaf rust fungus. BMC Plant Biology 18, 76
| Functional analysis of a pathogenesis-related thaumatin-like protein gene TaLr35PR5 from wheat induced by leaf rust fungus.Crossref | GoogleScholarGoogle Scholar | 29728059PubMed |
Žofajová A, Pšenáková I, Havrlentová M, Piliarová M (2012) Accumulation of total anthocyanins in wheat grain. Agriculture (Pol’nohospodárstvo) 58, 50–56.
| Accumulation of total anthocyanins in wheat grain.Crossref | GoogleScholarGoogle Scholar |
