Artemisinin and Ambrosia trifida extract aggravate the effects of short freeze–thaw stress in winter rye (Secale cereale) seedlings
Jiancai Guo A , Guozhang Bao![https://orcid.org/0000-0003-0329-8001](/media/client/orcid_16x16.png)
A Key Laboratory of Groundwater Resources and Environment of the Ministry of Education (Jilin University); Jilin Provincial Key Laboratory of Water Resources and Environment; College of New Energy and Environment, Jilin University, Changchun 130012, China.
B College of Biological and Agricultural Engineering, Jilin University, Changchun 130012, China.
C The Administration of Jingyu Water Conservation, Jingyu 135200, China.
D Yushu Forestry and Grassland Comprehensive Service Center, Yushu 815000, China.
Functional Plant Biology 50(6) 497-506 https://doi.org/10.1071/FP22271
Submitted: 9 November 2022 Accepted: 11 April 2023 Published: 28 April 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
The freeze–thaw and allelopathy from alien giant ragweed (Ambrosia trifida L.) and artemisinin have led to a serious stress to plants, influencing the agricultural quality and crop yield in north-east China. Yet, little is known how allelopathy affect plants under the freeze–thaw process. In this study, the characteristics in winter rye (Secale cereale L.) seedlings were investigated by laboratory simulation. The results showed that during the freezing process, application of artemisinin and A. trifida extract significantly increased the soluble protein content and accelerated lipid peroxidation, while they significantly inhibited antioxidant enzymes, photosynthesis and respiration (P < 0.05). During the thawing process, the freezing pressure decreased, and activities of antioxidant enzymes were significantly improved to mitigate artemisinin and A. trifida extract induced stress (P < 0.05). In addition, the sensitivity of the investigated metabolic processes in winter rye seedlings were highest to artemisinin and A. trifida extract in the freezing process. This study suggested that the stress response induced by artemisinin and A. trifida extract on winter rye seedlings in the freezing process was greater than that in the thawing process.
Keywords: allelopathy, artemisinin, combined stress, freeze–thaw, giant ragweed, plant physiology, tolerance, winter rye.
References
Aftab T, Khan MMA, Naeem M, Idrees M, Moinuddin Teixeira da Silva JA, Ram M (2012) Exogenous nitric oxide donor protects Artemisia annua from oxidative stress generated by boron and aluminium toxicity. Ecotoxicology and Environmental Safety 80, 60–68.| Exogenous nitric oxide donor protects Artemisia annua from oxidative stress generated by boron and aluminium toxicity.Crossref | GoogleScholarGoogle Scholar |
Araus JL, Sanchez-Bragado R, Vicente R (2021) Improving crop yield and resilience through optimization of photosynthesis: panacea or pipe dream. Journal of Experimental Botany 72, 3936–3955.
| Improving crop yield and resilience through optimization of photosynthesis: panacea or pipe dream.Crossref | GoogleScholarGoogle Scholar |
Arora R (2018) Mechanism of freeze–thaw injury and recovery: a cool retrospective and warming up to new ideas. Plant Science 270, 301–313.
| Mechanism of freeze–thaw injury and recovery: a cool retrospective and warming up to new ideas.Crossref | GoogleScholarGoogle Scholar |
Bao G, Tang W, An Q, Liu Y, Tian J, Zhao N, Zhu S (2020) Physiological effects of the combined stresses of freezing-thawing, acid precipitation and deicing salt on alfalfa seedlings. BMC Plant Biology 20, 204–212.
| Physiological effects of the combined stresses of freezing-thawing, acid precipitation and deicing salt on alfalfa seedlings.Crossref | GoogleScholarGoogle Scholar |
Ben Jaballah S, Zribi I, Haouala R (2017) Physiological and biochemical responses of two lentil varieties to chickpea (Cicer arietinum L.) aqueous extracts. Scientia Horticulturae 225, 74–80.
| Physiological and biochemical responses of two lentil varieties to chickpea (Cicer arietinum L.) aqueous extracts.Crossref | GoogleScholarGoogle Scholar |
Bian W, Bao G, Qian H, Song Z, Qi Z, Zhang M, Chen W, Dong W (2018) Physiological response characteristics in Medicago sativa under freeze-thaw and deicing salt stress. Water Air & Soil Pollution 229, 196
| Physiological response characteristics in Medicago sativa under freeze-thaw and deicing salt stress.Crossref | GoogleScholarGoogle Scholar |
Blum A (2014) The abiotic stress response and adaptation of triticale – a review. Cereal Research Communications 42, 359–375.
| The abiotic stress response and adaptation of triticale – a review.Crossref | GoogleScholarGoogle Scholar |
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 |
Bruce Williamson G, Richardson D (1988) Bioassays for allelopathy: measuring treatment responses with independent controls. Journal of Chemical Ecology 14, 181–187.
| Bioassays for allelopathy: measuring treatment responses with independent controls.Crossref | GoogleScholarGoogle Scholar |
Cantwell MI, Hong G, Albornoz K, Berlanga M (2022) Fresh grapevine (Vitis vinifera L.) leaves: postharvest biology and handling recommendations. Scientia Horticulturae 292, 110627
| Fresh grapevine (Vitis vinifera L.) leaves: postharvest biology and handling recommendations.Crossref | GoogleScholarGoogle Scholar |
Chang Y, Zhang J, Bao G, Yan B, Qu Y, Zhang M, Tang W (2021) Physiological responses of highland barley seedlings to NaCl, drought, and freeze-thaw stress. Journal of Plant Growth Regulation 40, 154–161.
| Physiological responses of highland barley seedlings to NaCl, drought, and freeze-thaw stress.Crossref | GoogleScholarGoogle Scholar |
Chen K, Renaut J, Sergeant K, Wei H, Arora R (2013) Proteomic changes associated with freeze-thaw injury and post-thaw recovery in onion (Allium cepa L.) scales. Plant, Cell & Environment 36, 892–905.
| Proteomic changes associated with freeze-thaw injury and post-thaw recovery in onion (Allium cepa L.) scales.Crossref | GoogleScholarGoogle Scholar |
Chen Y, Jiang J, Chang Q, Gu C, Song A, Chen S, Dong B, Chen F (2014) Cold acclimation induces freezing tolerance via antioxidative enzymes, proline metabolism and gene expression changes in two chrysanthemum species. Molecular Biology Reports 41, 815–822.
| Cold acclimation induces freezing tolerance via antioxidative enzymes, proline metabolism and gene expression changes in two chrysanthemum species.Crossref | GoogleScholarGoogle Scholar |
Gęgotek A, Skrzydlewska E (2019) Biological effect of protein modifications by lipid peroxidation products. Chemistry and Physics of Lipids 221, 46–52.
| Biological effect of protein modifications by lipid peroxidation products.Crossref | GoogleScholarGoogle Scholar |
Gong Z, Chen W, Bao G, Sun J, Ding X, Fan C (2020) Physiological response of Secale cereale L. seedlings under freezing-thawing and alkaline salt stress. Environmental Science and Pollution Research 27, 1499–1507.
| Physiological response of Secale cereale L. seedlings under freezing-thawing and alkaline salt stress.Crossref | GoogleScholarGoogle Scholar |
Griffith M, Ala P, Yang DS, Hon WC, Moffatt BA (1992) Antifreeze protein produced endogenously in winter rye leaves. Plant Physiology 100, 593–596.
| Antifreeze protein produced endogenously in winter rye leaves.Crossref | GoogleScholarGoogle Scholar |
Hájek J, Váczi P, Barták M, Jahnová L (2012) Interspecific differences in cryoresistance of lichen symbiotic algae of genus Trebouxia assessed by cell viability and chlorophyll fluorescence. Cryobiology 64, 215–222.
| Interspecific differences in cryoresistance of lichen symbiotic algae of genus Trebouxia assessed by cell viability and chlorophyll fluorescence.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 |
Hu T, Zhao T, Zhao K, Shi J (2019) A continuous global record of near-surface soil freeze/thaw status from AMSR-E and AMSR2 data. International Journal of Remote Sensing 40, 6993–7016.
| A continuous global record of near-surface soil freeze/thaw status from AMSR-E and AMSR2 data.Crossref | GoogleScholarGoogle Scholar |
Huang JH, Fu R, Liang CX, Dong DF, Luo XL (2010) Allelopathic effects of cassava (Manihot esculenta crantz) on radish (Raphanus sativus L.) and ryegrass (Lolium perenne L.). Allelopathy Journal 25, 155–162.
Ikkonen EN, Shibaeva TG, Sherudilo EG, Titov AF (2020) Response of winter wheat seedlings respiration to long-term cold exposure and short-term daily temperature drops. Russian Journal of Plant Physiology 67, 538–544.
| Response of winter wheat seedlings respiration to long-term cold exposure and short-term daily temperature drops.Crossref | GoogleScholarGoogle Scholar |
Iqbal MF, Feng WW, Guan M, Xiang LZ, Feng YL (2020) Biological control of natural herbivores on Ambrosia trifida species at liaoning province in northeast china. Applied Ecology and Environmental Research 18, 1419–1436.
| Biological control of natural herbivores on Ambrosia trifida species at liaoning province in northeast china.Crossref | GoogleScholarGoogle Scholar |
Jessing KK, Cedergreen N, Jensen J, Hansen HCB (2009) Degradation and ecotoxicity of the biomedical drug artemisinin in soil. Environmental Toxicology and Chemistry 28, 701–710.
| Degradation and ecotoxicity of the biomedical drug artemisinin in soil.Crossref | GoogleScholarGoogle Scholar |
Kong CH, Wang P, Xu XH (2007) Allelopathic interference of Ambrosia trifida with wheat (Triticum aestivum). Agriculture, Ecosystems & Environment 119, 416–420.
| Allelopathic interference of Ambrosia trifida with wheat (Triticum aestivum).Crossref | GoogleScholarGoogle Scholar |
Lang J, Barták M, Hájek J, Váczi P, Zikmundová B (2020) Chilling effects on primary photosynthetic processes in Medicago sativa: acclimatory changes after short- and long-term exposure to low temperatures. Biologia 75, 1105–1114.
| Chilling effects on primary photosynthetic processes in Medicago sativa: acclimatory changes after short- and long-term exposure to low temperatures.Crossref | GoogleScholarGoogle Scholar |
Liu H, Bao G, Dou Z, Liu H, Bai J, Chen Y, Yuan Y, Zhang X, Xi J (2022) Response characteristics of highland barley under freeze-thaw, drought and artemisinin stresses. BMC Plant Biology 22, 126
| Response characteristics of highland barley under freeze-thaw, drought and artemisinin stresses.Crossref | GoogleScholarGoogle Scholar |
Morvillo CM, de la Fuente EB, Gil A, Martínez-Ghersa MA, González-Andújar JL (2011) Competitive and allelopathic interference between soybean crop and annual wormwood (Artemisia annua L.) under field conditions. European Journal of Agronomy 34, 211–221.
| Competitive and allelopathic interference between soybean crop and annual wormwood (Artemisia annua L.) under field conditions.Crossref | GoogleScholarGoogle Scholar |
Muscolo A, Panuccio MR, Sidari M (2001) The effect of phenols on respiratory enzymes in seed germination. Plant Growth Regulation 35, 31–35.
| The effect of phenols on respiratory enzymes in seed germination.Crossref | GoogleScholarGoogle Scholar |
Ni L, Acharya K, Hao X, Li S, Li Y, Li Y (2012) Effects of artemisinin on photosystem II performance of Microcystis aeruginosa by in vivo chlorophyll fluorescence. Bulletin of Environmental Contamination and Toxicology 89, 1165–1169.
| Effects of artemisinin on photosystem II performance of Microcystis aeruginosa by in vivo chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar |
Pierpoint WS (2004) The extraction of enzymes from plant tissues rich in phenolic compounds. Methods in Molecular Biology 244, 65–74.
| The extraction of enzymes from plant tissues rich in phenolic compounds.Crossref | GoogleScholarGoogle Scholar |
Popov VN, Antipina OV, Trunova TI (2010) Lipid peroxidation during low-temperature adaptation of cold-sensitive tobacco leaves and roots. Russian Journal of Plant Physiology 57, 144–147.
| Lipid peroxidation during low-temperature adaptation of cold-sensitive tobacco leaves and roots.Crossref | GoogleScholarGoogle Scholar |
Pu Y, Liu L, Wu J, Zhao Y, Bai J, Ma L, Yue J, Jin J, Niu Z, Fang Y, Sun W (2019) Transcriptome profile analysis of winter rapeseed (Brassica napus L.) in response to freezing stress, reveal potentially connected events to freezing stress. International Journal of Molecular Sciences 20, 2771
| Transcriptome profile analysis of winter rapeseed (Brassica napus L.) in response to freezing stress, reveal potentially connected events to freezing stress.Crossref | GoogleScholarGoogle Scholar |
Qu Y, Bao G, Pan X, Bao L, Guo J, Xi J, Zhang X, Yang Y, Zhao H, Li G (2022) Response characteristics of highland barley (Hordeum vulgare) seedlings to the stress of salinity and artemisinin under freeze–thaw environment. Functional Plant Biology 49, 958–969.
| Response characteristics of highland barley (Hordeum vulgare) seedlings to the stress of salinity and artemisinin under freeze–thaw environment.Crossref | GoogleScholarGoogle Scholar |
Ramazan S, Qazi HA, Dar ZA, John R (2021) Low temperature elicits differential biochemical and antioxidant responses in maize (Zea mays) genotypes with different susceptibility to low temperature stress. Physiology and Molecular Biology of Plants 27, 1395–1412.
| Low temperature elicits differential biochemical and antioxidant responses in maize (Zea mays) genotypes with different susceptibility to low temperature stress.Crossref | GoogleScholarGoogle Scholar |
Šoln K, Klemenčič M, Koce JD (2022) Plant cell responses to allelopathy: from oxidative stress to programmed cell death. Protoplasma 259, 1111–1124.
| Plant cell responses to allelopathy: from oxidative stress to programmed cell death.Crossref | GoogleScholarGoogle Scholar |
Su P, Liu X, Wang R, Liu T, Zhao W, Sun M, Wang H, Liu Y, Wu Q (2022) Autotoxicity of Ambrosia artemisiifolia and Ambrosia trifida and its significance for the regulation of intraspecific populations density. Scientific Reports 12, 17424
| Autotoxicity of Ambrosia artemisiifolia and Ambrosia trifida and its significance for the regulation of intraspecific populations density.Crossref | GoogleScholarGoogle Scholar |
Šućur J, Konstantinović B, Crnković M, Bursić V, Samardžić N, Malenčić Đ, Prvulović D, Popov M, Vuković G (2021) Chemical composition of Ambrosia trifida L. and its allelopathic influence on crops. Plants 10, 2222
| Chemical composition of Ambrosia trifida L. and its allelopathic influence on crops.Crossref | GoogleScholarGoogle Scholar |
Tang W, Bao G, Yan B, Qu Y, Guo J, Zhu S, Zhao H (2021) Responses of barley seedlings to salinity and drought under freeze-thaw conditions. Applied Ecology and Environmental Research 19, 1909–1923.
| Responses of barley seedlings to salinity and drought under freeze-thaw conditions.Crossref | GoogleScholarGoogle Scholar |
Wu R, Wu B, Cheng H, Wang S, Wei M, Wang C (2021) Drought enhanced the allelopathy of goldenrod on the seed germination and seedling growth performance of lettuce. Polish Journal of Environmental Studies 30, 423–432.
| Drought enhanced the allelopathy of goldenrod on the seed germination and seedling growth performance of lettuce.Crossref | GoogleScholarGoogle Scholar |
Xu K, Zhao Y, Gu J, Zhou M, Gao L, Sun RX, Wang WW, Zhang SH, Yang XJ (2022) Proteomic analysis reveals the molecular mechanism underlying the cold acclimation and freezing tolerance of wheat (Triticum aestivum L.). Plant Science 318, 111242
| Proteomic analysis reveals the molecular mechanism underlying the cold acclimation and freezing tolerance of wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar |
Yan ZQ, Wang DD, Ding L, Cui HY, Jin H, Yang XY, Yang JS, Qin B (2015) Mechanism of artemisinin phytotoxicity action: induction of reactive oxygen species and cell death in lettuce seedlings. Plant Physiology and Biochemistry 88, 53–59.
| Mechanism of artemisinin phytotoxicity action: induction of reactive oxygen species and cell death in lettuce seedlings.Crossref | GoogleScholarGoogle Scholar |
Yin B, Li J, Zhang Q, Wu N, Zhang J, Rong X, Tao Y, Zang Y, Li Y, Zhou X, Zhang Y (2021) Freeze-thaw cycles change the physiological sensitivity of Syntrichia caninervis to snow cover. Journal of Plant Physiology 266, 153528
| Freeze-thaw cycles change the physiological sensitivity of Syntrichia caninervis to snow cover.Crossref | GoogleScholarGoogle Scholar |
Zhang T, Barry RG, Knowles K, Ling F, Armstrong RL (2003) Distribution of seasonally and perennially frozen ground in the Northern Hemisphere. Permafrost 2, 1289–1294.
Zhang B, Wang Y, Wu C, Qiu S, Chen X, Cai B, Xie H (2021) Freeze-thawing impairs the motility, plasma membrane integrity and mitochondria function of boar spermatozoa through generating excessive ROS. BMC Veterinary Research 17, 127–135.
| Freeze-thawing impairs the motility, plasma membrane integrity and mitochondria function of boar spermatozoa through generating excessive ROS.Crossref | GoogleScholarGoogle Scholar |