Skip to main content

Advertisement

SpringerLink
Log in

Humic Acid as a Biostimulant in Improving Drought Tolerance in Wheat: the Expression Patterns of Drought-Related Genes

  • Original Article
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

A Correction to this article was published on 13 November 2021

This article has been updated

Abstract

Plants develop a series of physiological, biochemical, and molecular responses to survive in drought stress. Many drought-related genes with various functions which regulated by ABA-dependent and independent pathways have been identified in wheat. However, studies on the effect of biostimulants on drought-related genes are limited and unclear. As a biostimulant, humic acid (HA) has enormous roles on plant growth, yield, and protection of resistance in various abiotic stresses, but its relation to drought-related genes is unknown. Here, we aimed to determine the relationships between drought stress generated by − 6 bar and − 8 bar PEG6000 and ABA and HA treatments on total oxidant status (TOS) and total antioxidant status (TAS) and expression of miRNA target genes (AP2, GRF, LAC, CSD1/CSD2, and Plastocyanin) on tolerant (Aksel 2000 and Kırkpınar 79) and susceptible (Atlı 2002 and Kırmızı Kılçık) bread wheat (Triticum aestivum L.) genotypes. According to the results, the expression of the genes varied depending on genotype and tissue and it was determined whether the genes used ABA-dependent or ABA-independent mechanisms to provide tolerance to stress in our promoter analysis. Also, the irregularities of the biochemical changes and expression of genes that were caused by PEG6000 could be improved by HA considering the positive effects on genes.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data Availability

The authors are sure that all data and materials their published claims and comply with field standards.

Change history

References

  • Abiri R, Shaharuddin NA, Maziah M, Yusof ZNB, Atabaki N, Sahebi M, Hanafi MM (2017) Role of ethylene and the APETALA 2/ethylene response factor superfamily in rice under various abiotic and biotic stress conditions. Environ Exp Bot 134:33–44

    Article  CAS  Google Scholar 

  • Addo Quaye C, Eshoo TW, Bartel DP, Axtell MJ (2008) Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr Biol 18:758–762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Akdogan G, Tufekci ED, Uranbey S, Unver T (2016) miRNA-based drought regulation in wheat. Funct Integr Genomics 16:221–233

    Article  CAS  PubMed  Google Scholar 

  • Alptekin B, Langridge P, Budak H (2017) Abiotic stress miRNomes in the Triticeae. Funct Integr Genomics 17:145–170

    Article  CAS  PubMed  Google Scholar 

  • Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aydin A, Kant C, Turan M (2012) Humic acid application alleviate salinity stress of bean (Phaseolus vulgaris L ) plants decreasing membrane leakage. Afr J Agric Res 7:1073–1086

    Google Scholar 

  • Berbara RL, García AC (2014) Humic substances and plant defense metabolism. In Physiological mechanisms and adaptation strategies in plants under changing environment Springer, New York, NY pp 297–319

  • Berthet S, Thevenin J, Baratiny D, Demont-Caulet N, Debeaujon I, Bidzinski P, Lapierre C (2012) Role of plant laccases in lignin polymerization. Adv Bot Res 61:145–172

    Article  CAS  Google Scholar 

  • Budak H, Kantar M, Kurtoglu KY (2013) Drought tolerance in modern and wild wheat. Hindawi Publishing Corporation:1–16

  • Burkhead JL, Reynolds KA, Abdel Ghany SE, Cohu CM, Pilon M (2009) Copper homeostasis. New Phytol 182:799–816

    Article  CAS  PubMed  Google Scholar 

  • Chu CC, Lee WC, Guo WY, Pan SM, Chen LJ, Li HM, Jinn TL (2005) A copper chaperone for superoxide dismutase that confers three types of copper/zinc superoxide dismutase activity in Arabidopsis. Plant Physiol 139:425–436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cordeiro FC, Santa-Catarina C, Silveira V, Souza SRD (2011) Humic acid effect on catalase activity and the generation of reactive oxygen species in corn (Zea mays). Biosci Biotechnol Biochem 75:70–74

    Article  CAS  PubMed  Google Scholar 

  • Delfine S, Tognetti R, Desiderio E, Alvino A (2005) Effect of foliar application of N and humic acids on growth and yield of durum wheat. Agron Sustain Dev 25:183–191

    Article  CAS  Google Scholar 

  • Divi UK, Krishna P (2009) Brassinosteroid: a biotechnological target for enhancing crop yield and stress tolerance. New Biotechnol 26:131–136

    Article  CAS  Google Scholar 

  • Dong CJ, Liu JY (2010) The Arabidopsis EAR-motif-containing protein RAP2 1 functions as an active transcriptional repressor to keep stress responses under tight control. BMC Plant Biol 10:47

    Article  PubMed  PubMed Central  Google Scholar 

  • Dong Z, Liu H, Yang X (2018) Effects of drought stress on some physiological and biochemical indexes of wheat seedlings. Asian J Bot 1:11–19

    Google Scholar 

  • Dugas D, Bartel B (2008) Sucrose induction of Arabidopsis miR398 represses two Cu/Zn superoxide dismutases. Plant Mol Biol 67:403–417

    Article  CAS  PubMed  Google Scholar 

  • Eldem V, Akcay UC, Ozhuner E, Bakir Y, Uranbey S, Unver T (2012) Genome-wide identification of miRNAs responsive to drought in peach (Prunus persica) by highthroughput deep sequencing. PLoS One 7:14

    Article  Google Scholar 

  • Fujita Y, Yoshida T, Yamaguchi Shinozaki K (2013) Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiol Plant 147:15–27

    Article  CAS  PubMed  Google Scholar 

  • Garcia AC, Olaetxea M, Santos LA, Mora V, Baigorri R, Fuentes M, Zammareno AM, Berbera RLL, Garcia Mina JM (2016) Involvement of hormone-and ROS-signaling pathways in the beneficial action of humic substances on plants growing under normal and stressing conditions. Biomed Res Int 3747501:1–13

    Google Scholar 

  • Garcia-Mina JM, Antolín MC, Sanchez-Diaz M (2004) Metal-humic complexes and plant micronutrient uptake: a study based on different plant species cultivated in diverse soil types. Plant Soil 258:57–68

    Article  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Drought tolerance in wheat the scientific world journal. Plant Physiol Biochem 48:909–930

    Article  CAS  Google Scholar 

  • Guo Z, Ou WZ, Lu SY, Zhong Q (2006) Differential responses of antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. Plant Physiol Biochem 44:828–836

    Article  CAS  Google Scholar 

  • Hajyzadeh M, Turktas M, Khawar KM, Unver T (2015) miR408 overexpression causes increased drought tolerance in chickpea. Gene 555:186–193

    Article  CAS  PubMed  Google Scholar 

  • Hernández R, García A, Portuondo L, Muñiz S, Berbara R, Izquierdo F (2012) Protección antioxidativa de los ácidos húmicos extraídos de vermicompost en arroz (Oryza sativa L.) var. Rev Protección Veg 27:102–110

    Google Scholar 

  • Hoagland DR, Arnon DI (1938) The water-culture method for growing plants without soil. Univ Calif Coll Agric Exp Sta Circ Berkeley, CA:347–353

  • Huang SQ, Peng J, Qiu CX, Yang ZM (2009) Heavy metal-regulated new microRNAs from rice. J Inorg Biochem 103:282–287

    Article  CAS  PubMed  Google Scholar 

  • Huat CB, Nadarajah K, Ratnam W (2014, 1614) Identification of drought-responsive microRNAs in leaf and stem tissues of Oryza sativa by Solexa sequencing. In AIP Conference Proceedings:587–590

  • Hwang EW, Shin SJ, Park SC, Jeong MJ, Kwon HB (2011) Identification of miR172 family members and their putative targets responding to drought stress in Solanum tuberosum. Genes Genom 33:105–110

    Article  CAS  Google Scholar 

  • Jia X, Wang WX, Ren L, Chen XJ, Mendu V, Willcut B, Dinkins R, Tang X, Tang G (2009) Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populus tremula and Arabidopsis thaliana. Plant Mol Biol 71:51–59

    Article  CAS  PubMed  Google Scholar 

  • Jiang M, Zhang J (2002) Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot 53:2401–2410

    Article  CAS  PubMed  Google Scholar 

  • Kaur A, Gupta OP, Meena NL, Grewal A, Sharma P (2017) Comparative temporal expression analysis of MicroRNAs and their target genes in contrasting wheat genotypes during osmotic stress. Appl Biochem Biotechnol 181:613–626

    Article  CAS  PubMed  Google Scholar 

  • Khan S, Bano A, Uddin J, Gurmani AR (2012) Abscisic acid and salicylic acid seed treatment as potent inducer of drought tolerance in wheat (Triticum aestivum L.). Pak J Bot 44:43–49

    CAS  Google Scholar 

  • Kim JS, Mizoi J, Kidokoro S, Maruyama K, Nakajima J, Nakashima K, Yoshizumi T (2012) Arabidopsis growth-regulating factor7 functions as a transcriptional repressor of abscisic acid–and osmotic stress–responsive genes, including DREB2A. Plant Cell 24:3393–3405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar D, Singh D, Kanodia P, Prabhu KV, Kumar M, Mukhopadhyay K (2014) Discovery of novel leaf rust responsive microRNAs in wheat and prediction of their target genes. J Nucleic Acids 570176

  • Le Roy J, Blervacq AS, Créach A, Huss B, Hawkins S, Neutelings G (2017) Spatial regulation of monolignol biosynthesis and laccase genes control developmental and stress-related lignin in flax. BMC Plant Biol 17:124

    Article  PubMed  PubMed Central  Google Scholar 

  • Li T, Li H, Zhang YX, Liu JY (2010) Identification and analysis of seven HO-responsive miRNAs and 32 new miRNAs in the seedlings of rice (Oryza sativa L. ssp. indica). Nucleic Acids Res 39:2821–2833

    Article  PubMed  PubMed Central  Google Scholar 

  • Li B, Qin Y, Duan H, Yin W, Xia X (2011) Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica. J Exp Bot 62:3765–3779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li D, Luo Z, Mou W, Wang Y, Ying T, Mao L (2014) ABA and UV-C effects on quality, antioxidant capacity and anthocyanin contents of strawberry fruit (Fragaria ananassa Duch.). Postharvest Biol Technol 90:56–62

    Article  CAS  Google Scholar 

  • Liang G, Ai Q, Yu D (2015) Uncovering miRNAs involved in crosstalk between nutrient deficiencies in Arabidopsis. Sci Rep 5:11813

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu D, Song Y, Chen Z, Yu D (2009) Ectopic expression of miR396 suppresses GRF target gene expression and alters leaf growth in Arabidopsis. Physiol Plant 136:223–236

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Able AJ, Able JA (2016) Water-deficit stress-responsive microRNAs and their targets in four durum wheat genotypes. Funct Int Genom:1–15

  • Liu S, Lv Z, Liu Y, Li L, Zhang L (2018) Network analysis of ABA-dependent and ABA-independent drought responsive genes in Arabidopsis thaliana. Genet Mol Biol 41:624–637

    Article  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Ma C, Burd S, Lers A (2015) miR408 is involved in abiotic stress responses in Arabidopsis. Plant J 84:169–187

    Article  CAS  PubMed  Google Scholar 

  • Mallory AC, Bartel DP, Bartel B (2005) MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17:1360–1375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michel BE, Kaufmann MR (1973) The osmotic potential of polyethyline glycol 6000. Plant Physiol 51:914–916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mora V, Olaetxea M, Bacaicoa E, Baigorri R, Fuentes M, Zamarreño AM, Garcia Mina JM (2014) Abiotic stress tolerance in plants: exploring the role of nitric oxide and humic substances in nitric oxide in plants: metabolism and role in stress physiology. Springer, Cham:243–264

  • Morris KV, Mattick JS (2014) The rise of regulatory RNA. Nat Rev Genet 15:423–437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moura JCMS, Bonine CAV, de Oliveira Fernandes Viana J, Dornelas MC, Mazzafera P (2010) Abiotic and biotic stresses and changes in the lignin content and composition in plants. J Integr Plant Biol 52:360–376

    Article  CAS  PubMed  Google Scholar 

  • Mutum RD, Balyan SC, Kansal S, Agarwal P, Kumar S, Kumar M, Raghuvanshi S (2013) Evolution of variety-specific regulatory schema for expression of osa-miR408 in indica rice varieties under drought stress. FEBS J 280:1717–1730

    Article  CAS  PubMed  Google Scholar 

  • Nezhadahmadi A, Prodhan ZH, Faruq G (2013) Drought tolerance in wheat. Sci World J 2013:1–12

    Article  Google Scholar 

  • Pan Y, Seymour GB, Lu C, Hu Z, Chen X, Chen G (2012) An ethylene response factor (ERF5) promoting adaptation to drought and salt tolerance in tomato. Plant Cell Rep 31:349–360

    Article  CAS  PubMed  Google Scholar 

  • Pandey GK, Grant JJ, Cheong YH, Kim BG, Li L, Luan S (2005) ABR1, an APETALA2-domain transcription factor that functions as a repressor of ABA response in Arabidopsis. Plant Physiol 139:1185–1193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paul S, Gayen D, Datta SK, Datta K (2016) Analysis of high iron rice lines reveals new miRNAs that target iron transporters in roots. J Exp Bot 67:5811–5824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pourcel L, Routaboul JM, Cheynier V, Lepiniec L, Debeaujon I (2007) Flavonoid oxidation in plants: from biochemical properties to physiological functions. Trends Plant Sci 12:29–36

    Article  CAS  PubMed  Google Scholar 

  • Rao S, Ftz J (2013) In vitro selection and characterization of polyethylene glycol (PEG) tolerant callus lines and regeneration of plantlets from the selected callus lines in sugarcane (Saccharum officinarum L.). Physiol Mol Biol Plants 19:261–268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ren J, Sun LN, Zhang QY, Song XS (2016) Drought tolerance is correlated with the activity of antioxidant enzymes in Cerasus humilis seedlings. Biomed Res Int 9851095:1–9

    Google Scholar 

  • Russell L, Stokes AR, Macdonald H, Muscolo A, Nardi S (2006) Stomatal responses to humic substances and auxin are sensitive to inhibitors of phospholipase A2. Plant Soil 283:175–185

    Article  CAS  Google Scholar 

  • Sairam RK, Srivastava GC, Agarwal S, Meena RC (2005) Differences in antioxidant activity in response to salinity stress in tolerant and susceptible wheat genotypes. Biol Plant 49:85–91

    Article  CAS  Google Scholar 

  • Shamimuzzaman M, Vodkin L (2012) Identification of soybean seed developmental stage-specific and tissue-specific miRNA targets by degradome sequencing. BMC Genomics 13:310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen J, Xie K, Xiong L (2010) Global expression profiling of rice microRNAs by one-tube stem-loop reverse transcription quantitative PCR revealed important roles of microRNAs in abiotic stress responses. Mol Gen Genomics 284:477–488

    Article  CAS  Google Scholar 

  • Sunkar R, Girke T, Jain PK, Zhu JK (2005) Cloning and characterization of microRNAs from rice. Plant Cell 17:1397–1411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tahir MM, Khurshid M, Khan MZ, Abbasi MK, Kazmi MH (2011) Lignite-derived humic acid effect on growth of wheat plants in different soils. Pedosphere 21:124–131

    Article  CAS  Google Scholar 

  • Trindade I, Capitão C, Dalmay T, Fevereiro MP, Dos Santos DM (2010) miR398 and miR408 are up-regulated in response to water deficit in Medicago truncatula. Planta 231:705–716

    Article  CAS  PubMed  Google Scholar 

  • Turlapati PV, Kim KW, Davin LB, Lewis NG (2011) The laccase multigene family in Arabidopsis thaliana: towards addressing the mystery of their gene function(s). Planta 233:439–470

    Article  CAS  PubMed  Google Scholar 

  • Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci U S A 97:11632–11637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang M, Wang Q, Zhang B (2013) Response of miRNAs and their targets to salt and drought stresses in cotton (Gossypium hirsutum L.). Gene 530:26–32

    Article  CAS  PubMed  Google Scholar 

  • Wei L, Wang L, Yang Y, Liu G, Wu Y, Guo T, Kang G (2015) Abscisic acid increases leaf starch content of polyethylene glycol-treated wheat seedlings by temporally increasing transcripts of genes encoding starch synthesis enzymes. Acta Physiol Plant 37(10):206

    Article  Google Scholar 

  • Yamaguchi Shinozaki K, Shinozaki K (2005) Organization of cis acting elements in osmotic and cols stres responsive promoters. Trends Plant Sci 10:88–94

    Article  CAS  PubMed  Google Scholar 

  • Yamasaki H, Abdel Ghany SE, Cohu CM, Kobayashi Y, Shikanai T, Pilon M (2007) Regulation of copper homeostasis by micro-RNA in Arabidopsis. J Biol Chem 282:16369–16378

    Article  CAS  PubMed  Google Scholar 

  • Yildirim N, Agar G, Taspinar MS, Turan M, Aydin M, Arslan E (2014) Protective role of humic acids against dicamba-induced genotoxicity and DNA methylation in Phaseolus vulgaris L. Acta Agr Scand B-S P 64:141–148

    CAS  Google Scholar 

  • Zhang A, Jiang M, Zhang J, Tan M, Hu X (2006) Mitogen-activated protein kinase is involved in abscisic acid-induced antioxidant defense and acts downstream of reactive oxygen species production in leaves of maize plants. Plant Physiol 141:475–487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang S, Zhou J, Han S, Yang W, Li W, Wei H, Li X, Qi L (2010) Four abiotic stress-induced miRNA families differentially regulated in the embryogenic and non-embryogenic callus tissues of Larix leptolepis. Biochem Bioph Res Co 398:355–360

    Article  CAS  Google Scholar 

  • Zhang YC, Yu Y, Wang CY, Li ZY, Liu Q, Xu J, Xin P (2013) Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nat Biotechnol 31:848–854

    Article  CAS  PubMed  Google Scholar 

  • Zhang JP, Yu Y, Feng YZ, Zhou YF, Zhang F, Yang YW (2017) Mir408 regulates grain yield and photosynthesis via a phytocyanin protein. Plant Physiol 175:1175–1185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Song Z, Li F, Li X, Ji H, Yang S (2019) The specific MYB binding sites bound by TaMYB in the GAPCp2/3 promoters are involved in the drought stress response in wheat. BMC Plant Biol 19(1):366

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhong YP, Li Z, Bai DF, Qi XJ, Chen JY, Wei CG, Lin MM, Fang JB (2018) In vitro variation of drought tolerance in five actinidia species. J Am Soc Hortic Sci 143:226–234

    Article  Google Scholar 

  • Zlatev ZS, Lidon FC, Ramalho JC, Yordanov IT (2006) Comparison of resistance to drought of three bean cultivars. Biol Plant 50:389–394

    Article  CAS  Google Scholar 

Download references

Funding

This study was funded by Ataturk University Research Funds (project no: 2015/346).

Author information

Authors and Affiliations

  1. Department of Biology, Faculty of Science, Ataturk University, 25240, Erzurum, Turkey

    Esra Arslan & Guleray Agar

  2. Department of Agricultural Biotechnology, Faculty of Agriculture, Ataturk University, 25240, Erzurum, Turkey

    Murat Aydin

Authors
  1. Esra Arslan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guleray Agar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Murat Aydin
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

E. Arslan and M. Aydin performed the measurements and wrote the manuscript. G. Agar participated in the planning of the study, data analysis, and writing of the manuscript.

Corresponding author

Correspondence to Esra Arslan.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethics Approval

Not applicable.

Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Code Availability

All authors are sure that all software application or custom code support their published claims and comply with field standards.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Key Message

Drought is becoming a threat to the effect of increasing global warming. Wheat is an important and necessary food for the growing human population. The effect of humic acid was determined on some drought-related and ABA-dependent or independent gene expressions.

Supplementary Information

Table S1

The cis-acting elements present in the promoter region of the AP2 (PDF 115 kb)

Table S2

The cis-acting elements present in the promoter region of the GRF (PDF 223 kb)

Table S3

The cis-acting elements present in the promoter region of the LAC (PDF 147 kb)

Table S4

The cis-acting elements present in the promoter region of the CSD1/CSD2 (PDF 240 kb)

Table S5

The cis-acting elements present in the promoter region of the Plastocyanin (PDF 221 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Arslan, E., Agar, G. & Aydin, M. Humic Acid as a Biostimulant in Improving Drought Tolerance in Wheat: the Expression Patterns of Drought-Related Genes. Plant Mol Biol Rep 39, 508–519 (2021). https://doi.org/10.1007/s11105-020-01266-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-020-01266-3

Keywords

Search

Navigation