Differences of endogenous polyamines and putative genes associated with paraquat resistance in goosegrass (Eleusine indica L.)


Autoři: Qiyu Luo aff001;  Jiping Wei aff001;  Zhaoxia Dong aff001;  Xuefeng Shen aff001;  Yong Chen aff001
Působiště autorů: Department of Crop Cultivation and Farming System, South China Agricultural University, Guangzhou, Guangdong, China aff001
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0216513

Souhrn

Background

Paraquat is one of the most effective herbicides used to control weeds in agricultural management, while the pernicious weed goosegrass (Eleusine indica) has evolved resistance to herbicides, including paraquat. Polyamines provide high-level paraquat resistance in many plants. In the present study, we selected three polyamines, namely, putrescine, spermidine, and spermine, as putative genes to investigate their correlation with paraquat resistance by using paraquat-resistant (R) and paraquat-susceptible (S) goosegrass populations.

Results

There was no significant difference in the putrescine nor spermine content between the R and S biotypes. However, 30 and 90 min after paraquat treatment, the spermidine concentration was 346.14-fold and 421.04-fold (P < 0.001) higher in the R biotype than in the S biotype, but the spermidine concentration was drastically reduced to a marginal level after 90 min. Since the transcript level of PqE was low while the spermidine concentration showed a transient increase, the PqE gene was likely involved in the synthesis of the paraquat resistance mechanism, regulation of polyamine content, and synthesis of spermidine and spermine. PqTS1, PqTS2, and PqTS3 encode transporter proteins involved in the regulation of paraquat concentration but showed different transcription patterns with synchronous changes in polyamine content.

Conclusion

Endogenous polyamines (especially spermidine) play a vital role in paraquat resistance in goosegrass. PqE, PqTS1, PqTS2, and PqTS3 were speculated on the relationship between polyamine metabolism and paraquat resistance. To validate the roles of PqE, PqTS1, PqTS2, and PqTS3 in polyamine transport systems, further research is needed.

Klíčová slova:

Cell membranes – Herbicides – High performance liquid chromatography – Polymerase chain reaction – Reverse transcriptase-polymerase chain reaction – Seedlings – Toxicity – Weeds


Zdroje

1. Jung HI, Kuk YI, Kim HY, Back K, Lee DJ, Lee S, et al. Resistance levels and fitness of protoporphyrinogen oxidase (PROTOX) inhibitor-resistant transgenic rice in paddy fields. Field Crops Res. 2010;115: 125–131.

2. Jóri B, Soós V, Szegő D, Páldi E, Szigeti Z, Rácz I, et al. Role of transporters in paraquat resistance of horseweed Conyza canadensis (L.) cronq. Pestic Biochem Physiol. 2007;88: 57–65.

3. Dong S, Hu H, Wang Y, Xu Z, Zha Y, Cai X, et al. A pqr2 mutant encodes a defective polyamine transporter and is negatively affected by ABA for paraquat resistance in Arabidopsis thaliana. J Plant Res. 2016;129: 899–907. doi: 10.1007/s10265-016-0819-y 27229891

4. Xi J, Xu P and Xiang CB. Loss of AtPDR11, a plasma membrane-localized ABC transporter, confers paraquat tolerance in Arabidopsis thaliana. Plant J.2012; 69: 782–791. doi: 10.1111/j.1365-313X.2011.04830.x 22026747

5. Tseng T, Ou J and Wang C. Role of the ascorbate–glutathione cycle in paraquat tolerance of rice. Weed Sci. 2013;61: 361–373.

6. Tsuji K, Hosokawa M, Morita S, Miura R, Tominaga T and Kudsk P. Resistance to paraquat in Mazus pumilus. Weed Res. 2013; 53: 176–182.

7. Powles SB and Yu Q. Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol. 2010; 61:317–347. doi: 10.1146/annurev-arplant-042809-112119 20192743

8. Hawkes TR. Mechanisms of resistance of paraquat in plants. Pest Management Science. 2014; 70:1316–1323. doi: 10.1002/ps.3699 24307186

9. Li J, Mu J, Bai J, Fu F, Zou T, An F, et al. Paraquat resistant1, a golgi-localized putative transporter protein, is involved in intracellular transport of paraquat. Plant Physiol. 2013;162: 470–483. doi: 10.1104/pp.113.213892 23471133

10. Zhang C, Feng L and Tian XS. Alterations in the 5' untranslated region of the 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) gene influence EPSPS overexpression in glyphosate-resistant Eleusine indica. Pestic Manage Sci. 2018;74: 2561–2568.

11. Lii R, Steed S and Stall W. Confirmation and control of a paraquat-tolerant goosegrass (Eleusine indica) biotype. Weed Technol. 2002;16: 309–313.

12. Seng C, Lun L, Chathye S and Sahid I. Initial report of glufosinate and paraquat multiple resistance that evolved in a biotype of goosegrass (Eleusine indica) in Malaysia. Weed Biol Manag. 2010;10: 229–233.

13. An J, Shen X, Ma Q, Yang C, Liu S and Chen Y. Transcriptome profiling to discover putative genes associated with paraquat resistance in goosegrass (Eleusine indica L.). PLoS One. 2014; 9: e99940. doi: 10.1371/journal.pone.0099940 24927422

14. Pandolfi C, Pottosin I, Cuin T, Mancuso S and Shabala S. Specificity of polyamine effects on NaCl-induced ion flux kinetics and salt stress amelioration in plants. Plant Cell Physiol. 2010; 51: 422–434. doi: 10.1093/pcp/pcq007 20061303

15. Hart JJ, Ditomaso JM, Linscott DL and Kochian LV. Transport interactions between Paraquat and polyamines in roots of intact maize seedlings. Plant Physiol. 1992;99: 1400–1405. doi: 10.1104/pp.99.4.1400 16669051

16. Benavides M, Gallego S, Comba M and Tomaro M. Relationship between polyamines and paraquat toxicity in sunflower leaf discs. Plant Growth Regul. 2000; 31:215–224.

17. Chang C and Kao C. Paraquat toxicity is reduced by polyamines in rice leaves. Plant Growth Regul 22:163–168 (1997).

18. Alca´zar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C et al. Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta. 2010; 231:1237–1249. doi: 10.1007/s00425-010-1130-0 20221631

19. Mulangi V, Chibucos MC, Phuntumart V, Morris PF. Kinetic and phylogenetic analysis of plant polyamine uptake trasnsporters. Planta. 2012; 236:1261–1273. doi: 10.1007/s00425-012-1668-0 22711282

20. Dinis-Oliveira RJ, Duarte JA, Sanchez-Navarro A, Remiao F, Bastos ML and Carvalho F. Paraquat poisonings: mechanisms of lung toxicity, clinical features, and treatment. Crit Rev Toxicol. 2008;38: 13–71. doi: 10.1080/10408440701669959 18161502

21. Szigeti Z. Mechanism of paraquat resistance-from the antioxidant enzymes to the transporters. Acta Biol Szeged. 2005;49: 177–179.

22. Soar CJ, Preston C, Karotam J and Powles SB. Polyamines can inhibit paraquat toxicity and translocation in the broadleaf weed Arctotheca calendula. Pestic Biochem Physiol. 2004;80: 94–105.

23. Shen X, Hu F, Chen Y, Li Y and Han C. Preliminary study on resistance level of Eleusine indica to paraquat. Southwest China Journal of Agricultural Sciences. 2016;29: 1875–1878.

24. Altschul SF, Gish W, Miller W, Myers EW and Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215: 403–410. doi: 10.1016/S0022-2836(05)80360-2 2231712

25. Thompson JD, Higgins DG, Gibson TJ and Clustal W. Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22: 4673–4680. doi: 10.1093/nar/22.22.4673 7984417

26. Flores HE and Galston AW. Analysis of polyamines in higher plants by high performance liquid chromatography. Plant Physiol. 1982;69: 701–706. doi: 10.1104/pp.69.3.701 16662279

27. Wang F and Xue Y. Measurement of polyamine contents in plant tissue. Plant Physiol Commun 1988;1: 39–41.

28. Fujita M, Fujita Y, Iuchi S, Yamada K, Kobayashi Y, Urano K, et al. Natural variation in a polyamine transporter determines paraquat tolerance in Arabidopsis. Proc Natl Acad Sci USA 2012;109: 6343–6347. doi: 10.1073/pnas.1121406109 22492932

29. Brunharo CA and Hanson Bradley. Vacuolar sequestration of paraquat is involved in the resistance mechanism in Lolium perenne L. spp. multiflorum. 2017; 8:1485

30. Yu Q, Huang S and Powles S. Direct measurement of paraquat in leaf protoplasts indicates vacuolar paraquat sequestration as a resistance mechanism in Lolium rigidum. Pest Management. Biochemistry. Physiology. 2010; 98:104–109.

31. Kurepa J, Smalle J, Van Montagu M and Inze D. Polyamines and paraquat toxicity in Arabidopsis thaliana. Plant Cell Physiol. 1998;39: 987–992. doi: 10.1093/oxfordjournals.pcp.a029463 9816679

32. Kiyono M, Oka Y, Sone Y, Nakamura R, Sato MH, Sakabe K, et al. Bacterial heavy metal transporter MERC increases mercury accumulation in Arabidopsis thaliana. Biochem Eng J. 2013;71: 19–24.

33. Kiyono M, Oka Y, Sone Y, Tanaka M, Nakamura R, Sato MH, et al. Expression of the bacterial heavy metal transporter MERC fused with a plant SNARE, SYP121, in Arabidopsis thaliana increases cadmium accumulation and tolerance. Planta. 2012; 235: 841–850. doi: 10.1007/s00425-011-1543-4 22089884

34. Wen X, Gibson CJ, Yang I, Buckley B, Goedken MJ, Richardson JR et al. MDR1 transporter protects against paraquat-induced toxicity in human and mouse proximal tubule cells. Toxicol Sci. 2014;141:475–483. doi: 10.1093/toxsci/kfu141 25015657

35. Hart JJ, Ditomaso JM, Linscott DL and Kochian LV. Investigations into the cation specificity and metabolic requirements for paraquat transport in roots of intact maize seedlings. Pestic Biochem Physiol. 1993;45: 62–71.

36. Kashiwagi K, Hosokawa N, Furuchi T, Kobayashi H, Sasakawa C, Yoshikawa M, et al. Isolation of polyamine transport-deficient mutants of Escherichia coli and cloning of the genes for polyamine transport proteins. J Biol Chem. 1990;265: 20893–20897. 2249996


Článek vyšel v časopise

PLOS One


2019 Číslo 12