Investigation of the Role of Some Antioxidant Enzymes in the Relationship Between Drought Tolerance and Herbicide Resistance in Red Root Amaranth (Amaranthus retroflexus L.)

Abstract

Abiotic stresses reduce crop yield of plants via morphological, physiological, biochemical, and molecular changes. Drought stress increases reactive oxygen species (ROS) concentrations in the cell, damaging to phospholipids, proteins, and nucleic acids and resulting in chlorosis. Red root amaranth (Amaranthus retroflexus L.) is drought-resistant, summer annual, and herbaceous plant. It is common along roadsides, cultivated areas, and orchards. Herbicides such as 2,4-D, dicamba, mecoprop, bromoxynil, glyphosate are effective on A. retroflexus but many studies report the development of herbicide resistance in this species. In this study, it has been focused on determining some physiological and biochemical responses of A. retroflexus to short-term drought stress and glyphosate. For this purpose, total chlorophyll, total protein, lipid peroxidation (MDA), H2O2 (Hydrogen peroxide) amount, cell membrane permeability (electrolyte leakage), APX (Ascorbate peroxidase), and GR (Glutatyon reductase) activities were determined in leaf tissue of 21-day-old A. retroflexus seedlings. Drought stress and glyphosate treatments increased H2O2 and cell membrane permeability and resulting chlorosis in A. retroflexus. Our results showed that A. retroflexus had high ROS damage and low ROS scavenging activity after glyphosate treatment. This indicates that A. retroflexus is sensitive to glyphosate based on antioxidant capacity. In addition, this research shows for the first time how short-term drought stress and glyphosate affect APX and GR activities in A. retroflexus. As a result, it was determined that oxidative stress causes more damage with glyphosate compared to short-term drought in A. retroflexus.

Keywords

• Amaranthus retroflexus
• Glyphosate
• Drought stress
• APX
• GR

Kızılbacak (Amaranthus retroflexus L.) Bitkisinde Kuraklık Toleransı ve Herbisit Direnci Arasındaki İlişkide Bazı Antioksidan Enzimlerin Rolünün Araştırılması

Abstract

Abiyotik stresler bitkide morfolojik, fizyolojik, biyokimyasal ve moleküler değişiklikler yoluyla ürün verimini düşürür. Kuraklık stresi, hücredeki reaktif oksijen türlerinin (ROT) konsantrasyonlarını arttırarak hücredeki fosfolipidlere, proteinlere ve nükleik asitlere zarar verir, klorozla sonuçlanır. Yazlık bir yabancı ot olan kızılbacak (Amaranthus retroflexus L.) kuraklığa dayanıklı, tek yıllık ve otsu bir bitkidir. Yol kenarları, ekili alanlar ve meyve bahçelerinde yaygındır. 2,4-D, dicamba, mecoprop, bromoxynil, glifosat gibi herbisitler A. retroflexus üzerinde etkilidir. Ancak birçok çalışma bu türde herbisit direncinin geliştiğini bildirmektedir. Bu araştırma, kısa süreli kuraklık ve glyphosate’ın A. retroflexus’ta neden olduğu bazı fizyolojik ve biyokimyasal yanıtlara odaklanmıştır. Bu amaçla, 21 günlük A. retroflexus fidelerinin yaprak dokusunda toplam klorofil, toplam protein, lipit peroksidasyon (MDA), H2O2 (Hidrojen peroksit) miktarı, hücre zarı geçirgenliği (elektrolit sızıntısı), APX (Askorbat peroksidaz) ve GR (Glutatyon redüktaz) aktiviteleri belirlenmiştir. Kuraklık stresi ve glifosat A. retroflexus’ta H2O2 miktarını ve hücre zarı geçirgenliğini arttırmış ve kloroza neden olmuştur. Sonuçlarımız A. retroflexus’a glifosat uygulaması sonrasında yüksek ROT zararı ve düşük ROT temizleme aktivitesi olduğunu göstermiştir. Bu, antioksidan kapasite temelinde A. retroflexus’un glyphosate’a duyarlı olduğuna işaret etmektedir. Ayrıca bu araştırma ile A. retroflexus’ta kuraklık ve glyphosate’ın APX ve GR aktivitelerini nasıl etkilediği ilk defa gösterilmektedir. Sonuçta, A. retroflexus’ta oksidatif stresin kısa süreli kuraklığa kıyasla glifosat ile daha çok zarara neden olduğu saptanmıştır.

Keywords

• Amaranthus retroflexus
• glifosat
• Kuraklık stresi
• APX
• GR

References

1. Asada K. (1999). The water-water cycle in chloroplasts: Scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 1999; 50: 601-39.
2. Asadi S., Abadi HA., A-Zadeh PS. (2019). The effect of different irrigation periods on growth indicators of some weed species. Applied Ecology and Environmental Research 17(5):10929-10940.
3. Avashthi, H., Pathak RK., Gaur VS., Singh S., Gupta VK., Ramteke PW., Kumar A. (2020). Comparative analysis of ROS-scavenging gene families in finger millet, rice, sorghum, and foxtail millet revealed potential targets for antioxidant activity and drought tolerance improvement. Netw Model Anal Health Inform Bioinforma 9: 33.
4. Batra NG., Sharma V., Kumari N. (2014). Drought-induced changes in chlorophyll fluorescence, photosynthetic pigments, and thylakoid membrane proteins of Vigna Radiate. J. Plant Interact. 1: 712–721.
5. Botella MA., Rosado RA., Hasegawa PM. (2005). Plant adaptive responses to salinity stress. Plant Abiotic Stress, Blackwell Publishing Ltd, 270 p.
6. Boyer JS. (1982). Plant productivity and environment. Science, 218(4571): 443-448.
7. Bradford M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72: 248-254.
8. Büyük İ., Soydam-Aydın S., Aras S. (2012). Bitkilerin stres koşullarına verdiği moleküler cevaplar. Türk Hijyen ve Deneysel Biyoloji Dergisi, 69(2): 97-110.

9. Cheeseman JM. (2006). Hydrogen peroxide concentrations in leaves under natural conditions, J of Experimental Botany 57: 2435–44.
10. Davies KJA. (1987). Protein damage and degradation by oxygen radicals. I. General Aspects. J. Biol. Chem. 262: 9895-9901.
11. Demirbaş S., Acar O. 2008. Superoxide dismutase and peroxidase activities from antioxidative enzymes in Helianthus annuus L. roots during Orobanche cumana Wallr. Penetration. Fresenius Environ. Bull., 17 (8a): 1038-1044.
12. Dionisio-Sese ML., Tobita S. (1998). Antioxidant responses of rice seedlings to salinity stress. Plant Science, 135: 1-9.
13. Edreva A. (2005). Generation and scavenging of reactive oxygen species in chloroplasts: A submolecular approach. Agriculture, Ecosystems and Environment 106: 119–133.
14. Elstner EF., Osswald W. (1994), Mechanisms of oxygen activation during plant stress, Proc. R. Soc. Edinb., 102 B: 131-154.
15. Foyer CH., Descourvières P., Kunert KJ. (1994). Protection against oxygen radicals: An important defense mechanism studied in transgenic plants. Plant, Cell & Environment Journal, 17(5): 507–523.
16. Foyer CH., Halliwell B. (1976). Presence of Glutathione and Glutathione Reductase in Chloroplasts: A Proposed Role in Ascorbic Acid Metabolism. Planta, 133: 21-25.
17. Foyer CH., Noctor G. (2009). Redox regulation in photosynthetic organisms: Signaling, acclimation, and practical implications. Antioxidants & redox signaling, 11(4): 861-905.
18. Franz JE., Mao MK., Sikorski JA. (1997). Glyphosate: A unique global herbicide; American Chemical Society: Washington, DC, pp 521-527, 604-605, 615.
19. Hay MM., Dille JA., Peterson DE. (2019). Management of pigweed (Amaranthus spp.) in grain sorghum with integrated strategies. Weed Technology, 33(5): 701-709.
20. Huang Z., Huang H., Chen J., Chen J., Wei S., Zhang C. (2019). Nicosulfuron-Resistant Amaranthus retroflexus L. in Northeast China. Crop Protection, 122: 79-83.
21. Kadıoğlu İ., Başaran B., Kaya Y. (2015). Amaranthus retroflexus L.: An invasive plant. Türkiye Herboloji Dergisi, 18(3): 74-76.
22. Karimmojeni H., Bazrafshan AH., Majidi MM., Torabian S., Rashidi B. (2014). Effect of maternal nitrogen and drought stress on seed dormancy and germinability of Amaranthus retroflexus. Plant Species Biology, 29(3): E1-E8.
23. Lawrence KS. (2002). Herbicide Handbook, 8 th ed. Vencill, WK.(Ed), Weed Science Society of America, p 231-234.
24. Levitt J. (1980). Responses of Plants to Environmental Stresses. Academic Press, New York.
25. Madhava RKV., Sresty TVS. (2000). Antioxidative parameters in the seedlings of Pigeon pea (Cajanus cajan L. Millspaugh) in response to Zn and Ni stresses. Plant Sci., 157: 113-128.
26. Maroli AS., Nandula VK., Dayan FE., Duke SO., Gerard P., Tharayil N. (2015). Metabolic profiling and enzyme analyses indicate a potential role of antioxidant systems in complementing glyphosate resistance in an Amaranthus palmeri biotype. Journal of agricultural and food chemistry, 63(41): 9199-9209.
27. Masekoa I., Ncubec B., Mabhaudhia T., Tesfayb S., Chimonyoa VGP., Arayac HT., Fessehazionc M., Du Plooyc CP. (2019).
28. Moisture stress on physiology and yield of some indigenous leafy vegetables under field conditions. South African Journal of Botany, 126: 85-91.
29. Møller IM., Jensen PE., Hansson A. (2007). Oxidative modifications to cellular components in plants. Annu Rev Plant Biol, 58: 459-81.
30. Murphy BP., Larran AS., Ackley B., Loux MM., Tranel PJ., (2019). Survey of glyphosate, atrazine-and lactofen-resistance mechanisms in Ohio Waterhemp (Amaranthus tuberculatus) populations. Weed Science, 67(3): 296-302.
31. Nakano Y., Asada K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and cell physiology, 22(5): 867-880.
32. Özkur O., Ozdemir F., Bor M., Turkan I. (2009). Physiochemical and antioxidant responses of the perennial xerophyte Capparis ovata Desf. to drought. Environmental and experimental botany, 66(3): 487-492.
33. Peryea FJ., Kammereck R. (1997). Use of Minolta SPAD‐502 chlorophyll meter to quantify the effectiveness of mid‐summer trunk injection of iron on chlorotic pear trees. Journal of plant nutrition, 20(11): 1457-1463.
34. Saraswathi SG., Paliwal K. (2011). Drought induced changes in growth, leaf gas exchange and biomass production in Albizia lebbeck and Cassia siamea seedlings. Journal of environmental biology, 32(2): 173-178.
35. Sarker U., Oba S. (2018). Catalase, superoxide dismutase and ascorbate-glutathione cycle enzymes confer drought tolerance of Amaranthus tricolor. Scientific reports, 8(1): 1-12.
36. Slabbert MM., Krüger GHJ. (2014). Antioxidant enzyme activity, proline accumulation, leaf area and cell membrane stability in water stressed Amaranthus leaves. South African Journal of Botany, 95: 123-128.
37. Steward FC. (1983). Plant Physiology, Academic Press, New York and London, 797p.
38. Tomlin CDS. (2006). The pesticides manual: a world compendium. British Crop Protection Council, 14: 351.
39. Tozlu G., Çoruh İ., Gültekin L. (2010). Türkiye’de Amaranthus (Amaranthaceae) türlerine karşı biyolojik mücadelede böceklerin kullanımı. Atatürk Üniversitesi Ziraat Fakültesi Dergisi, 41(2): 169-176.
40. Valdayskikh, V.V., Voronin, P.Y., Artemyeva, E.P., Rymar, V.P. (2019). Amaranth responses to experimental soil drought. In AIP Conference Proceedings (Vol. 2063, No. 1, p. 030023). AIP Publishing LLC.
41. Vieira, B.C., Samuelson, S.L., Alves, G.S., Gaines, T.A., Werle, R., Kruger, G.R. (2018). Distribution of glyphosate‐resistant Amaranthus spp. in Nebraska. Pest management scie9nce, 74(10): 2316-2324.
42. WHO (1996). Data Sheets on Pesticides: Glyphosate; International Programme on Chemical Safety, World Health Organization, Food and Agriculture Organization: Geneva, Switzerland.
43. Zhang, H., Duan, W., Xie, B., Wang B., Hou F., Li A., Dong S., Qin Z., Wang Q., Zhang L. (2020). Root yield, antioxidant capacities, and hormone contents in different drought-tolerant sweet potato cultivars treated with ABA under early drought stress. Acta Physiol Plant 42: 132.
44. Zhang, H., Duan, W., Xie, B., Wang, B., Hou, F., Li, A., Zhang, L. (2020). Root yield, antioxidant capacities, and hormone contents in different drought-tolerant sweet potato cultivars treated with ABA under early drought stress. Acta Physiologiae Plantarum, 42(8): 1-15.