A gene that underwent adaptive evolution, LAC2 (LACCASE), in Populus euphratica improves drought tolerance by improving water transport capacity.

Zhimin Niu, Guiting Li, Hongyin Hu, Jiaojiao Lv, Qiwei Zheng, Jianquan Liu, Dongshi Wan
Author Information
  1. Zhimin Niu: State Key Laboratory of Grassland Agro-Ecosystem, School of Life Sciences, Lanzhou University, Lanzhou, Gansu, People's Republic of China.
  2. Guiting Li: State Key Laboratory of Grassland Agro-Ecosystem, School of Life Sciences, Lanzhou University, Lanzhou, Gansu, People's Republic of China.
  3. Hongyin Hu: State Key Laboratory of Grassland Agro-Ecosystem, School of Life Sciences, Lanzhou University, Lanzhou, Gansu, People's Republic of China.
  4. Jiaojiao Lv: State Key Laboratory of Grassland Agro-Ecosystem, School of Life Sciences, Lanzhou University, Lanzhou, Gansu, People's Republic of China.
  5. Qiwei Zheng: Laboratory of Cell Biology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, People's Republic of China.
  6. Jianquan Liu: State Key Laboratory of Grassland Agro-Ecosystem, School of Life Sciences, Lanzhou University, Lanzhou, Gansu, People's Republic of China.
  7. Dongshi Wan: State Key Laboratory of Grassland Agro-Ecosystem, School of Life Sciences, Lanzhou University, Lanzhou, Gansu, People's Republic of China. wandsh@lzu.edu.cn.

Abstract

Drought severely limits plant development and growth; accordingly, plants have evolved strategies to prevent water loss and adapt to water deficit conditions. However, experimental cases that corroborate these evolutionary processes are limited. The LACCASEs (LACs) family is involved in various plant development and growth processes. Here, we performed an evolutionary analysis of LACs from Populus euphratica and characterized the functions of LACs in Arabidopsis and poplar. The results showed that in PeuLACs, multiple gene duplications led to apparent functional redundancy as the result of various selective pressures. Among them, PeuLAC2 underwent strong positive selection. Heterologous expression analyses showed that the overexpression of PeuLAC2 alters the xylem structure of plants, including thickening the secondary cell wall (SCW) and increasing the fiber cell length and stem tensile strength. Altogether, these changes improve the water transport capacity of plants. The analysis of the physiological experimental results showed that PeuLAC2-OE lines exhibited a stronger antioxidant response and greater drought tolerance than WT. Three genes screened by transcriptome analysis, NAC025, BG1, and UGT, that are associated with SCW synthesis and drought stress were all upregulated in the PeuLAC2-OE lines, implying that the overexpression of PeuLAC2 thickened the SCW, improved the water transport capacity of the plant, and further enhanced its drought tolerance. Our study highlights that genes that have undergone adaptive evolution may participate in the development of adaptive traits in P. euphratica and that PeuLAC2 could be a candidate gene for molecular genetic breeding in trees.

References

  1. J Vis Exp. 2010 Mar 11;(37): [PMID: 20224547]
  2. Environ Sci Pollut Res Int. 2018 Nov;25(33):33103-33118 [PMID: 30284160]
  3. Tree Physiol. 2009 Oct;29(10):1237-46 [PMID: 19661134]
  4. Mol Biol Evol. 2007 Aug;24(8):1586-91 [PMID: 17483113]
  5. Nat Commun. 2013;4:2215 [PMID: 23896897]
  6. Nat Struct Biol. 2002 Aug;9(8):601-5 [PMID: 12118243]
  7. Biotechnol Biofuels. 2015 Sep 15;8:145 [PMID: 26379777]
  8. Cell. 2009 Feb 6;136(3):389-92 [PMID: 19203571]
  9. Plant Biotechnol J. 2014 Oct;12(8):1132-42 [PMID: 24975689]
  10. Eur J Biochem. 1990 Jan 26;187(2):341-52 [PMID: 2404764]
  11. J Exp Bot. 2006;57(11):2563-9 [PMID: 16804053]
  12. Int J Mol Sci. 2017 Jan 30;18(2): [PMID: 28146098]
  13. Plant Cell. 2018 Oct;30(10):2512-2528 [PMID: 30242037]
  14. Front Plant Sci. 2019 Sep 11;10:1083 [PMID: 31572409]
  15. Plant Cell. 2005 Nov;17(11):2966-80 [PMID: 16243908]
  16. Plant Physiol. 2002 May;129(1):145-55 [PMID: 12011346]
  17. Trends Plant Sci. 2010 Dec;15(12):664-74 [PMID: 20846898]
  18. Annu Rev Cell Dev Biol. 2006;22:53-78 [PMID: 16824006]
  19. Plant J. 1998 Dec;16(6):735-43 [PMID: 10069079]
  20. Planta. 2017 Jun;245(6):1091-1104 [PMID: 28214919]
  21. Plant Cell. 2011 Mar;23(3):1124-37 [PMID: 21447792]
  22. Curr Opin Biotechnol. 2010 Apr;21(2):197-203 [PMID: 20363612]
  23. Plant Cell. 2018 Nov;30(11):2649-2662 [PMID: 30341147]
  24. Phytochemistry. 2015 Apr;112:84-90 [PMID: 25236694]
  25. PLoS One. 2019 Feb 12;14(2):e0210892 [PMID: 30753186]
  26. F1000Res. 2016 Jun 30;5: [PMID: 27441087]
  27. Planta. 2011 Mar;233(3):439-70 [PMID: 21063888]
  28. Nat Commun. 2013;4:2797 [PMID: 24256998]
  29. Trends Plant Sci. 2005 Feb;10(2):79-87 [PMID: 15708345]
  30. Mol Plant Pathol. 2019 Mar;20(3):309-322 [PMID: 30267563]
  31. Nat Protoc. 2008;3(6):1101-8 [PMID: 18546601]
  32. Science. 1995 Oct 20;270(5235):368-9, 371 [PMID: 7569988]
  33. Plant Cell Environ. 2010 Dec;33(12):2101-11 [PMID: 20636490]
  34. Planta. 2006 Oct;224(5):1185-96 [PMID: 16779554]
  35. Plant Physiol. 2018 Feb;176(2):1808-1823 [PMID: 29229698]
  36. J Biomol Struct Dyn. 2015 Sep;33(9):1835-49 [PMID: 25301391]
  37. Plant Physiol. 2014 Feb;164(2):765-76 [PMID: 24394777]
  38. Genes (Basel). 2017 Dec 08;8(12): [PMID: 29292723]
  39. Gene. 2014 Nov 15;552(1):98-105 [PMID: 25218040]
  40. Mol Biol (Mosk). 2018 Jul-Aug;52(4):567-575 [PMID: 30113022]
  41. Genes (Basel). 2016 Dec 01;7(12): [PMID: 27916935]
  42. Front Plant Sci. 2012 May 07;3:85 [PMID: 22639669]
  43. Plant Biotechnol J. 2019 Feb;17(2):451-460 [PMID: 30044051]
  44. Biotechnol Lett. 2010 Sep;32(9):1325-32 [PMID: 20464449]
  45. Plant Cell. 2010 Aug;22(8):2660-79 [PMID: 20798329]
  46. Trends Plant Sci. 2004 Oct;9(10):490-8 [PMID: 15465684]
  47. Proc Natl Acad Sci U S A. 2013 Jun 25;110(26):10848-53 [PMID: 23754401]
  48. Plant Cell. 2013 Oct;25(10):3976-87 [PMID: 24143805]
  49. Sci Rep. 2016 Sep 08;6:32795 [PMID: 27605130]
  50. Nature. 2012 Nov 29;491(7426):752-5 [PMID: 23172141]
  51. Biochemistry (Mosc). 2012 Dec;77(12):1395-407 [PMID: 23244736]
  52. Am J Bot. 2007 May;94(5):709-15 [PMID: 21636440]
  53. J Vis Exp. 2010 Mar 12;(37): [PMID: 20228730]

Grants

  1. 31870580/National Natural Science Foundation of China (National Science Foundation of China)
  2. 31470620/National Natural Science Foundation of China (National Science Foundation of China)
  3. 31870580/National Natural Science Foundation of China (National Science Foundation of China)
  4. 31470620/National Natural Science Foundation of China (National Science Foundation of China)
  5. 31870580/National Natural Science Foundation of China (National Science Foundation of China)
  6. 31470620/National Natural Science Foundation of China (National Science Foundation of China)
  7. 31870580/National Natural Science Foundation of China (National Science Foundation of China)
  8. 31470620/National Natural Science Foundation of China (National Science Foundation of China)
  9. 31470620/National Natural Science Foundation of China (National Science Foundation of China)
  10. 31870580/National Natural Science Foundation of China (National Science Foundation of China)
  11. 31470620/National Natural Science Foundation of China (National Science Foundation of China)

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