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RESEARCH ARTICLE

The increased hydrocyanic acid in drought-stressed sorghums could be alleviated by plant growth regulators

A. A. Shehab A B , Luhua Yao A , Liangliang Wei A , Dengke Wang A , Yang Li A , Xuefeng Zhang A and Yanjun Guo https://orcid.org/0000-0002-7252-3041 A C
+ Author Affiliations
- Author Affiliations

A College of Agronomy and Biotechnology, Southwest University, Chongqing 400716, China.

B Department of Agronomy, Faculty of Agriculture, AL-Azhar University, Cairo 11651, Egypt.

C Corresponding author. Email: qhgyj@126.com

Crop and Pasture Science 71(5) 459-468 https://doi.org/10.1071/CP20057
Submitted: 19 February 2020  Accepted: 2 April 2020   Published: 13 May 2020

Abstract

Droughts not only reduce the biomass of sorghum (Sorghum bicolor (L.) Moench) but also increase the risk of hydrogen cyanide (HCN) toxicity to animals, mainly due to increased HCN content in drought-stressed plants. In the present study, the variations of HCN contents in 12 sorghum genotypes (10 sweet sorghum cultivars, one Sudangrass and one forage sorghum) were investigated at jointing, filling and ripening stages under rainfed conditions. Next, three genotypes – one sweet sorghum, one Sudangrass and one forage sorghum – were further selected to elucidate the physiological mechanisms of plant growth regulators (PGRs) (abscisic acid (ABA) and methyl jasmonate (MeJA)) in mitigating the concentrations of HCN in drought-stressed plants in a pot experiment. About 100 µg/L ABA and 100 µg/L MeJA were sprayed separately or together twice on drought-stressed (50 and 75% field water capacity) plant leaf. The drought lasted for 15 days. In the field experiment the HCN content in plants reduced from jointing to filling stages then increased from filling to ripening stages in several cultivars. In the pot experiment, drought increased the HCN accumulation and soluble protein content in leaves of all three genotypes. PGRs overall reduced the HCN contents in drought-stressed sweet sorghum and Sudangrass but not in forage sorghum (except in the ABA+MeJA treatment). However, the soluble protein contents were reduced by PGRs in drought-stressed forage sorghum but not in sweet sorghum (except in the ABA+MeJA treatment) and Sudangrass. Both ABA and MeJA increased the plant weights, whereas only MeJA enhanced net photosynthetic rate (PN) in all three genotypes. PGRs reduced release rate of superoxide and hydrogen peroxide and malondialdehyde in all drought-stressed plants, and reduced the activities of peroxidase, superoxide dismutase, catalase, and ascorbate peroxidase in sweet sorghum but not in other two genotypes. These results suggest that exogenous ABA and MeJA could increase plant weight and reduce HCN content in drought-stressed sorghums, with varying physiological responsive mechanisms among sorghum genotypes.

Additional keywords: ABA, anti-oxidative enzyme, forage, MeJA, Sorghum bicolor, water deficit.


References

Almodares A, Taheri R, Eraghizadeh F (2011) The effects of ethephon on biomass and carbohydrate content in two sweet sorghum cultivars. International Journal of Plant Production 5, 221–225.

Bano A, Ullah F, Nosheen A (2012) Role of abscisic acid and drought stress on the activities of antioxidant enzymes in wheat. Plant, Soil and Environment 58, 181–185.
Role of abscisic acid and drought stress on the activities of antioxidant enzymes in wheat.Crossref | GoogleScholarGoogle Scholar |

Bogatek R, Gawroñska H, Oracz K (2003) Involvement of oxidative stress and ABA in CN-mediated elimination of embryonic dormancy in apple. In ‘The biology of seeds: recent research advancement’. (Eds G Nicolas, KJ Bradford, D Come, HW Pritchard) pp. 211–216. (CABI Publishing: Wallingford, UK)

Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. The Plant Cell 7, 1099–1111.
Adaptations to environmental stresses.Crossref | GoogleScholarGoogle Scholar | 12242400PubMed |

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 942051PubMed |

Busk PK, Møller BL (2002) Dhurrin synthesis in sorghum is regulated at the transcriptional level and induced by nitrogen fertilization in older plants. Plant Physiology 129, 1222–1231.
Dhurrin synthesis in sorghum is regulated at the transcriptional level and induced by nitrogen fertilization in older plants.Crossref | GoogleScholarGoogle Scholar | 12114576PubMed |

De Geyter N, Gholami A, Goormachtig S, Goossens A (2012) Transcriptional machineries in jasmonate-elicited plant secondary metabolism. Trends in Plant Science 17, 349–359.
Transcriptional machineries in jasmonate-elicited plant secondary metabolism.Crossref | GoogleScholarGoogle Scholar | 22459758PubMed |

de Ollas C, Dodd IC (2016) Physiological impacts of ABA–JA interactions under water-limitation. Plant Molecular Biology 91, 641–650.
Physiological impacts of ABA–JA interactions under water-limitation.Crossref | GoogleScholarGoogle Scholar | 27299601PubMed |

Fugate KK, Lafta AM, Eide JD, Li G, Lulai EC, Olson L.L, Finger F.L (2018) Methyl jasmonate alleviates drought stress in young sugar beet (Beta vulgaris L.) plants. Journal of Agronomy and Crop Science 204, 566–576.
Methyl jasmonate alleviates drought stress in young sugar beet (Beta vulgaris L.) plants.Crossref | GoogleScholarGoogle Scholar |

Ganjewala D (2010) Advances in cyanogenic glycosides biosynthesis and analyses in plants: a review. Acta Biologica Szegediensis 54, 1–14.

Gleadow RM, Møller BL (2014) Cyanogenic glycosides: synthesis, physiology, and phenotypic plasticity. Annual Review of Plant Biology 65, 155–185.
Cyanogenic glycosides: synthesis, physiology, and phenotypic plasticity.Crossref | GoogleScholarGoogle Scholar | 24579992PubMed |

Gleadow RM, Ottman MJ, Kimball BA, Wall GW, Pinter PJ, LaMorte RL, Leavitt SW (2016) Drought-induced changes in nitrogen partitioning between cyanide and nitrate in leaves and stems of sorghum grown at elevated CO2 are age dependent. Field Crops Research 185, 97–102.
Drought-induced changes in nitrogen partitioning between cyanide and nitrate in leaves and stems of sorghum grown at elevated CO2 are age dependent.Crossref | GoogleScholarGoogle Scholar |

Gorz HJ, Haag WL, Specht JE, Haskins FA (1977) Assay of p-hydroxybenzaldehyde as a measure of hydrocyanic acid potential in sorghums. Crop Science 17, 578–582.
Assay of p-hydroxybenzaldehyde as a measure of hydrocyanic acid potential in sorghums.Crossref | GoogleScholarGoogle Scholar |

Haskins FA, Gorz HJ, Hill RM, Youngquist JB (1984) Influence of sample treatment on apparent hydrocyanic acid potential of sorghum leaf tissue. Crop Science 24, 1158–1163.
Influence of sample treatment on apparent hydrocyanic acid potential of sorghum leaf tissue.Crossref | GoogleScholarGoogle Scholar |

Hayes CM, Burow GB, Brown PJ, Thurber C, Xin Z, Burke JJ (2015) Natural variation in synthesis and catabolism genes influences dhurrin content in sorghum. The Plant Genome 8, 1–9.
Natural variation in synthesis and catabolism genes influences dhurrin content in sorghum.Crossref | GoogleScholarGoogle Scholar |

Hayes CM, Weers BD, Thakran M, Burow G, Xin Z, Emendack Y, Mullet JE (2016) Discovery of a dhurrin QTL in sorghum: co-localization of dhurrin biosynthesis and a novel stay-green QTL. Crop Science 56, 104–112.
Discovery of a dhurrin QTL in sorghum: co-localization of dhurrin biosynthesis and a novel stay-green QTL.Crossref | GoogleScholarGoogle Scholar |

Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207, 604–611.
Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds.Crossref | GoogleScholarGoogle Scholar |

Jana S, Choudhuri MA (1982) Glycolate metabolism of three submersed aquatic angiosperms during ageing. Aquatic Botany 12, 345–354.
Glycolate metabolism of three submersed aquatic angiosperms during ageing.Crossref | GoogleScholarGoogle Scholar |

Kautz S, Trisel JA, Ballhorn DJ (2014) Jasmonic acid enhances plant cyanogenesis and resistance to herbivory in lima bean. Journal of Chemical Ecology 40, 1186–1196.
Jasmonic acid enhances plant cyanogenesis and resistance to herbivory in lima bean.Crossref | GoogleScholarGoogle Scholar | 25399357PubMed |

Kubiś J (2008) Exogenous spermidine differentially alters activities of some scavenging system enzymes, H2O2 and superoxide radical levels in water-stressed cucumber leaves. Journal of Plant Physiology 165, 397–406.
Exogenous spermidine differentially alters activities of some scavenging system enzymes, H2O2 and superoxide radical levels in water-stressed cucumber leaves.Crossref | GoogleScholarGoogle Scholar | 17658660PubMed |

Lai D, Pičmanová M, Hachem MA, Motawia MS, Olsen CE, Møller BL, Takos AM (2015) Lotus japonicus flowers are defended by a cyanogenic β-glucosidase with highly restricted expression to essential reproductive organs. Plant Molecular Biology 89, 21–34.
Lotus japonicus flowers are defended by a cyanogenic β-glucosidase with highly restricted expression to essential reproductive organs.Crossref | GoogleScholarGoogle Scholar | 26249044PubMed |

Li Z, Li J, Du C, Huang H, Gong M (2002) Simultaneous measurement of five antioxidant enzyme activities using a single extraction system. Journal of Yunnan Normal University (Natural Sciences Edition) 22, 44–48.

Liu SW, Lv ZY, Liu YH, Li L, Zhang L (2018) Network analysis of ABA-dependent and ABA-independent drought responsive genes in Arabidopsis thaliana. Genetics and Molecular Biology 41, 624–637.
Network analysis of ABA-dependent and ABA-independent drought responsive genes in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Loyd RC, Gray E (1970) Amount and distribution of hydrocyanic acid potential during the life cycle of plants of three sorghum cultivars. Agronomy Journal 62, 394–397.
Amount and distribution of hydrocyanic acid potential during the life cycle of plants of three sorghum cultivars.Crossref | GoogleScholarGoogle Scholar |

Ma X, Ma F, Mi Y, Ma Y, Shu H (2008) Morphological and physiological responses of two contrasting Malus species to exogenous abscisic acid application. Plant Growth Regulation 56, 77
Morphological and physiological responses of two contrasting Malus species to exogenous abscisic acid application.Crossref | GoogleScholarGoogle Scholar |

Ma C, Wang ZQ, Zhang LT, Sun MM, Lin TB (2014) Photosynthetic responses of wheat (Triticum aestivum L.) to combined effects of drought and exogenous methyl jasmonate. Photosynthetica 52, 377–385.
Photosynthetic responses of wheat (Triticum aestivum L.) to combined effects of drought and exogenous methyl jasmonate.Crossref | GoogleScholarGoogle Scholar |

Meuriot F, Noquet C, Avice JC, Volenec JJ, Cunningham SM, Sors TG, Ourry A (2004) Methyl jasmonate alters N partitioning, N reserves accumulation and induces gene expression of a 32‐kDa vegetative storage protein that possesses chitinase activity in Medicago sativa taproots. Physiologia Plantarum 120, 113–123.
Methyl jasmonate alters N partitioning, N reserves accumulation and induces gene expression of a 32‐kDa vegetative storage protein that possesses chitinase activity in Medicago sativa taproots.Crossref | GoogleScholarGoogle Scholar | 15032883PubMed |

Miranshahi B, Sayyari M (2016) Methyl jasmonate mitigates drought stress injuries and affects essential oil of summer savory. Journal of Agricultural Science and Technology 1635–1645.

Moaveni P (2010) Effect of drought stress on dry forage yield, plant height, prussic acid and LAI in four varieties of Sorghum bicolor. In ‘2010 International Conference on Chemistry and Chemical Engineering’. Kyoto, Japan. pp. 395–397. (IEEE) 10.1109/iccceng.2010.5560406.

Mohanraj K, Gopalan A, Shanmuganathan M (2006) Genetic parameters for hydrocyanic acid content in forage sorghum (Sorghum bicolor L. Moench). Journal of Agricultural Sciences – Sri Lanka 2, 59–62.
Genetic parameters for hydrocyanic acid content in forage sorghum (Sorghum bicolor L. Moench).Crossref | GoogleScholarGoogle Scholar |

Naimah N, Jahan MS (2017) Signaling behaviour of abscisic acid on physiological activities in plants under stress. Pertanika. Journal of Tropical Agricultural Science 40, 485–496.

Najafi E, Pal I, Khanbilvardi R (2019) Climate drives variability and joint variability of global crop yields. Science of The Total Environment 662, 361–372.
Climate drives variability and joint variability of global crop yields.Crossref | GoogleScholarGoogle Scholar | 30690370PubMed |

O’Donnell NH, Møller BL, Neale AD, Hamill JD, Blomstedt CK, Gleadow RM (2013) Effects of PEG-induced osmotic stress on growth and dhurrin levels of forage sorghum. Plant Physiology and Biochemistry 73, 83–92.
Effects of PEG-induced osmotic stress on growth and dhurrin levels of forage sorghum.Crossref | GoogleScholarGoogle Scholar | 24080394PubMed |

Ohnishi N, Wacera F, Sakamoto W (2019) Photosynthetic responses to high temperature and strong light suggest potential post-flowering drought tolerance of sorghum Japanese Landrace Takakibi. Plant & Cell Physiology 60, 2086–2099.
Photosynthetic responses to high temperature and strong light suggest potential post-flowering drought tolerance of sorghum Japanese Landrace Takakibi.Crossref | GoogleScholarGoogle Scholar |

Pfeiffer BK, Pietsch D, Schnell RW, Rooney WL (2019) Long-term selection in hybrid sorghum breeding programs. Crop Science 59, 150–164.
Long-term selection in hybrid sorghum breeding programs.Crossref | GoogleScholarGoogle Scholar |

Phillips K, Ludidi N (2017) Drought and exogenous abscisic acid alter hydrogen peroxide accumulation and differentially regulate the expression of two maize RD22-like genes. Scientific Reports 7, 8821
Drought and exogenous abscisic acid alter hydrogen peroxide accumulation and differentially regulate the expression of two maize RD22-like genes.Crossref | GoogleScholarGoogle Scholar | 28821770PubMed |

Pičmanová M, Neilson EH, Motawia MS, Olsen CE, Agerbirk N, Gray CJ, Sánchez-Pérez RA (2015) Recycling pathway for cyanogenic glycosides evidenced by the comparative metabolic profiling in three cyanogenic plant species. Biochemical Journal 469, 375–389.
Recycling pathway for cyanogenic glycosides evidenced by the comparative metabolic profiling in three cyanogenic plant species.Crossref | GoogleScholarGoogle Scholar | 26205491PubMed |

Rademacher W (2015) Plant growth regulators: backgrounds and uses in plant production. Journal of Plant Growth Regulation 34, 845–872.
Plant growth regulators: backgrounds and uses in plant production.Crossref | GoogleScholarGoogle Scholar |

Roberts JA, Hooley R (1988) Commercial applications of PGRs – thought for food? In ‘Plant growth regulators. Tertiary level biology’. (Springer: Boston, MA, USA) 10.1007/978-1-4615-7592-4_11.

Saddhe AA, Kundan K, Padmanabh D (2017) Mechanism of ABA signaling in response to abiotic stress in plants. In ‘Mechanism of plant hormone signaling under stress, II’. (Ed. GK Pandey) pp. 173–195. (John Wiley & Sons Inc.: Hoboken, NJ, USA)

Sairam RK, Deshmukh PS, Shukla DS (1997) Tolerance of drought and temperature stress in relation to increased antioxidant enzyme activity in wheat. Journal of Agronomy & Crop Science 178, 171–178.
Tolerance of drought and temperature stress in relation to increased antioxidant enzyme activity in wheat.Crossref | GoogleScholarGoogle Scholar |

Schmidt FB, Cho SK, Olsen CE, Yang SW, Møller BL, Jørgensen K (2018) Diurnal regulation of cyanogenic glucoside biosynthesis and endogenous turnover in cassava. Plant Direct 2, e00038
Diurnal regulation of cyanogenic glucoside biosynthesis and endogenous turnover in cassava.Crossref | GoogleScholarGoogle Scholar | 31245705PubMed |

Sun Z, Zhang K, Chen C, Wu Y, Tang Y, Georgiev MI, Zhou M (2018) Biosynthesis and regulation of cyanogenic glycoside production in forage plants. Applied Microbiology and Biotechnology 102, 9–16.
Biosynthesis and regulation of cyanogenic glycoside production in forage plants.Crossref | GoogleScholarGoogle Scholar | 29022076PubMed |

Vos IA, Verhage A, Watt LG, Vlaardingerbroek I, Schuurink RC, Pieterse CMJ, Wees SCMV (2019) Abscisic acid is essential for rewiring of jasmonic acid-dependent defenses during herbivory. bioRxiv
Abscisic acid is essential for rewiring of jasmonic acid-dependent defenses during herbivory.Crossref | GoogleScholarGoogle Scholar |

Wang SY (1999) Methyl jasmonate reduces water stress in strawberry. Journal of Plant Growth Regulation 18, 127–134.
Methyl jasmonate reduces water stress in strawberry.Crossref | GoogleScholarGoogle Scholar | 10594248PubMed |

Wheeler JL, Mulcahy C, Walcott JJ, Rapp GG (1990) Factors affecting thehydrogen cyanide potential of forage sorghum. Australian Journal of Agricultural Research 41, 1093–1100.
Factors affecting thehydrogen cyanide potential of forage sorghum.Crossref | GoogleScholarGoogle Scholar |

Xia Q, He B, Liu YM, Xu J (2010) Effects of high temperature stress on the morphological and physiological characteristics in Scaevola albida cutting seedlings. Acta Ecologica Sinica 30, 5217–5224.

Yu X, Zhang W, Zhang Y, Zhang X, Lang D, Zhang X (2019) The roles of methyl jasmonate to stress in plants. Functional Plant Biology 46, 197–212.
The roles of methyl jasmonate to stress in plants.Crossref | GoogleScholarGoogle Scholar | 32172764PubMed |

Zahid A, Khanum A, Muhammad AM, Malik MA (2012) Effect of cutting and post-cutting intervals on hydrogen cyanide in sorghum forage grown under rain-fed conditions. Pakistan Journal of Botany 44, 955–960.

Zhao MR, Han YY, Feng YN, Li F, Wang W (2012) Expansins are involved in cell growth mediated by abscisic acid and indole-3-acetic acid under drought stress in wheat. Plant Cell Reports 31, 671–685.
Expansins are involved in cell growth mediated by abscisic acid and indole-3-acetic acid under drought stress in wheat.Crossref | GoogleScholarGoogle Scholar | 22076248PubMed |

Zhou M, Memelink J (2016) Jasmonate-responsive transcription factors regulating plant secondary metabolism. Biotechnology Advances 34, 441–449.
Jasmonate-responsive transcription factors regulating plant secondary metabolism.Crossref | GoogleScholarGoogle Scholar | 26876016PubMed |