Evidence for the Early Evolutionary Loss of the M20D Auxin Amidohydrolase Family from Mosses and Horizontal Gene Transfer from Soil Bacteria of Cryptic Hydrolase Orthologues to Physcomitrella patens

Abstract

Inactive auxin conjugates are accumulated in plants and hydrolyzed to recover phytohormone action. A family of metallopeptidase orthologues has been conserved in Plantae to help regulate auxin homeostatic levels during growth and development. This hydrolase family was recently traced back to liverwort, the most ancient extant land plant lineage. Liverwort’s auxin hydrolase has little activity against auxin conjugate substrates and does not appear to actively regulate auxin. This finding, along with data that shows moss can synthesize auxin conjugates, led to examining another bryophyte lineage, Physcomitrella patens. We have identified and isolated three M20D hydrolase paralogues from moss. The isolated enzymes strongly recognize and cleave a variety of auxin conjugates, including those of indole butyric and indole propionic acids. These P. patens hydrolases not only appear to be “cryptic”, but they are likely to have derived from soil bacteria through Horizontal Gene Transfer. Additionally, support is presented that the plant-type M20D peptidase family may have been universally lost from mosses after divergence from the common ancestor with liverwort.

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References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410

    CAS  Google Scholar 

  2. Bandurski RS, Cohen JD, Slovin JP, Reinecke DM (1995) Auxin biosynthesis and metabolism. In: Davies PJ (ed) Plant hormones, 2nd edn. Kluwer Academic Publishers, Boston, pp 39–65

    Google Scholar 

  3. Barkawi LS, Tam Y-Y, Tillman JA, Pederson B, Calio J, Al-Amier H, Emerick M, Normanly J, Cohen JD (2008) A high-throughput method for the quantitative analysis of indole-3-acetic acid and other auxins from plant tissue. Anal Biochem 372:177–188

    CAS  PubMed  Google Scholar 

  4. Bock R (2009) The give and take of DNA: horizontal gene transfer in plants. Trends Plant Sci 15(1):11–22

    PubMed  Google Scholar 

  5. Bray JR, Curtis JT (1957) An ordination of the upland forest of Southern Wisconsin. Ecol Monogr 27:325–349

    Google Scholar 

  6. Campanella JJ, Ludwig-Müller J, Town CD (1996) Isolation and characterization of mutants of Arabidopsis thaliana with increased resistance to growth inhibition by indoleacetic acid amino acid conjugates. Plant Physiol 112:735–745

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Campanella JJ, Ludwig-Müller J, Bakllamaja V, Sharma V, Cartier A (2003a) ILR1 and sILR1 IAA amidohydrolase homologues differ in expression pattern and substrate specificity. Plant Growth Regul 41:215–223

    CAS  Google Scholar 

  8. Campanella JJ, Bitincka L, Smalley JV (2003b) MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences. BMC Bioinform 4:29

    Google Scholar 

  9. Campanella JJ, Olajide A, Magnus V, Ludwig-Müller J (2004) A novel auxin conjugate from wheat with substrate specificity for longer side-chain auxin amide conjugates. Plant Physiol 135:2230–2240

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Campanella JJ, Smith SM, Leibu D, Wexler S, Ludwig-Müller J (2008) The auxin conjugate hydrolase family of Medicago truncatula and their expression during the interaction with two symbionts. J Plant Growth Regul 27(1):26–38

    CAS  Google Scholar 

  11. Campanella JJ, Kurdach K, Bochis J, Smalley JV (2018) Evidence for exaptation of the Marchantia polymorpha M20D peptidase MpILR1 into the tracheophyte auxin regulatory pathway. Plant Physiol 177(4):1595–1604

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Chou J-C, Mulbry WW, Cohen JD (2002) N-carbobenzyloxy-D-aspartic acid as a competitive inhibitor of indole-3-acetyl-L-aspartic acid hydrolase of Enterobacter agglomerans. Plant Growth Regul 37:241–248

    CAS  Google Scholar 

  13. Cohen JD, Baldi BG, Slovin JP (1986) 13C(6)-[benzene ring]-indole-3-acetic acid: a new internal standard for quantitative mass spectral analysis of indole-3-acetic acid in plants. Plant Physiol 80:14–19

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Cooke TJ, Poli DB, Sztein AE, Cohen JD (2002) Evolutionary patterns in auxin action. Plant Mol Biol 49:319–338

    CAS  PubMed  Google Scholar 

  15. Davies PJ (1995) Plant hormones: physiology, biochemistry and molecular biology. Klewer Academic Publishers, Dordrecht

    Google Scholar 

  16. Drábková LZ, Dobrev PI, Motyka V (2015) Phytohormone profiling across the bryophytes. PLoS ONE 10(5):e0125411

    Google Scholar 

  17. Fang H, Liexiang H, Rujia C, Pengcheng L, Shuhui X, Enying Z, Wei C, Liu L, Youli Y, Guohua L et al (2017) Ancestor of land plants acquired the DNA-3-methyladenine glycosylase (MAG) gene from bacteria through horizontal gene transfer. Sci Rep 7:9324

    PubMed  PubMed Central  Google Scholar 

  18. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Google Scholar 

  19. Geilfus C-M, Ludwig-Müller J, Bárdos G, Zörb C (2018) Early response to salt ions in maize (Zea mays L.). J Plant Physiol 220:173–180

    CAS  PubMed  Google Scholar 

  20. Gower JC (2015) Principal coordinates analysis. Wiley StatsRef: Statistics Reference Online, pp 1–7

  21. Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N, Seo M, Sato S, Yamada T, Mori H, Tajima N et al (2014) Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat Commun 5:3978–3986

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Kasahara H (2016) Current aspects of auxin biosynthesis in plants. Biosci Biotechnol Biochem 80(1):34–42

    CAS  PubMed  Google Scholar 

  23. Korasick DA, Enders TA, Strader LC (2013) Auxin biosynthesis and storage forms. J Exp Bot 64:2541–2555

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Lang D, Ullrich KK, Murat F, Fuchs J, Jenkins J, Haas FB, Piednoel M, Gundlach H, Van Bel M, Meyberg R et al (2018) The Physcomitrella patens chromosome-scale assembly reveals moss genome structure and evolution. Plant J 93(3):515–533

    CAS  PubMed  Google Scholar 

  25. Leong SS, Chiu W-C, Chou J-C (2009) Gene cloning, nucleotide analysis, and overexpression in Escherichia coli of a substrate-specific indole-3-acetyl-L-alanine hydrolase from. Arthrobacter ilicis. Bot Stud 50:11–20

    CAS  Google Scholar 

  26. Ligrone R, Duckett JG, Renzaglia KS (2012) Major transitions in the evolution of early land plants: a bryological perspective. Ann Bot 109:851–871

    PubMed  PubMed Central  Google Scholar 

  27. Ljung K, Hull AK, Kowalczyk M, Marchant A, Celenza J, Cohen JD, Sandberg G (2002) Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana. Plant Mol Biol 49:249–272

    CAS  PubMed  Google Scholar 

  28. Lu H, Zhao WM, Zheng Y (2005) Analysis of synonymous codon usage bias in Chlamydia. Acta Biochim Biophys Sin (Shanghai) 37(1):1–10

    CAS  Google Scholar 

  29. Ludwig-Müller J (2011) Auxin conjugates: their role for plant development and in the evolution of land plants. J Exp Bot 62:1757–1773

    PubMed  Google Scholar 

  30. Ludwig-Müller J, Decker EL, Reski R (2009a) Dead end for auxin conjugates in Physcomitrella? Plant Signal Behav 4:116–118

    PubMed  PubMed Central  Google Scholar 

  31. Ludwig-Müller J, Jülke S, Bierfreund NM, Decker EL, Reski R (2009b) Moss (Physcomitrella patens) GH3 proteins act in auxin homeostasis. New Phytol 181(2):323–338

    PubMed  Google Scholar 

  32. Matasci N, Hung L-H, Yan Z, Carpenter EJ, Wickett NJ, Mirarab S, Nguyen N, Warnow T, Ayyampalayam S, Barker M et al (2014) Data access for the 1,000 plants (1KP) project. GigaScience 3:17

    PubMed  PubMed Central  Google Scholar 

  33. Novak O, Hényková E, Sairanen I, Kowalczyk M, Pospíšil T, Ljung K (2012) Tissue-specific profiling of the Arabidopsis thaliana auxin metabolome. Plant J 72(3):523–536

    CAS  PubMed  Google Scholar 

  34. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn P, Minchin D, O’Hara PR, Simpson RB, Solymos GL P (2016) Vegan: community ecology package. R package version 2.4-1

  35. Ortiz-Ramírez C, Hernandez-Coronado M, Thamm A. Catarino B, Wang M, Dolan L, Feijó JAA, Becker JDD (2016) A transcriptome atlas of Physcomitrella patens provides insights into the evolution and development of land plants. Mol Plant 9:205–220

    PubMed  Google Scholar 

  36. Page RD (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    CAS  PubMed  Google Scholar 

  37. Qiu Y-L, Li L, Wang B, Chen Z, Knoop V, Groth-Malonek M, Dombrovska O, Lee J, Kent L, Rest J et al (2006) The deepest divergences in land plants inferred from phylogenomic evidence. Proc Natl Acad Sci USA 103:15511–15516

    CAS  PubMed  Google Scholar 

  38. Qiu Y-L, Li L, Wang B, Chen Z, Dombrovska O, Lee J, Kent L, Li R, Jobson RW, Hendry T, Taylor DW et al (2007) A nonflowering land plant phylogeny inferred from nucleotide sequences of seven chloroplast, mitochondrial, and nuclear genes. Int J Plant Sci 168:691–708

    CAS  Google Scholar 

  39. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  40. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud PF, Lindquist EA, Kamisugi Y (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319(5859):64–69

    CAS  PubMed  Google Scholar 

  41. Rowsell S, Pauptit RA, Tucker AD, Melton RG, Blow DM, Brick P (1997) Crystal structure of carboxypeptidase G2, a bacterial enzyme with applications in cancer therapy. Structure 15:337–347

    Google Scholar 

  42. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  43. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  44. Sauer M, Robert S, Kleine-Vehn J (2013) Auxin: simply complicated. J Exp Bot 64(9):2565–2577

    CAS  PubMed  Google Scholar 

  45. Shen XX, Hittinger CT, Rokas A (2017) Contentious relationships in phylogenomic studies can be driven by a handful of genes. Nat Ecol Evol 1(5):126

    PubMed  PubMed Central  Google Scholar 

  46. Smolko A, Ludwig-Müller J, Salopek-Sondi B (2018) Auxin amidohydrolases—from structure to function: revisited. Croat Chem Acta 91(2):233–239

    Google Scholar 

  47. Sztein AE, Cohen JD, García de la Fuente I, Cooke TJ (1999) Auxin metabolism in mosses and liverworts. Am J Bot 86:1544–1555

    CAS  Google Scholar 

  48. Sztein AE, Cohen JD, Cooke TJ (2000) Evolutionary patterns in the auxin metabolism of green plants. Int J Plant Sci 161:849–859

    CAS  Google Scholar 

  49. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4872–4882

    Google Scholar 

  50. Wellman CH, Osterloff PL, Mohiuddin U (2003) Fragments of the earliest land plants. Nature 425:282–285

    CAS  PubMed  Google Scholar 

  51. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York

    Google Scholar 

  52. Yu P, Lor P, Ludwig-Müller J, Hegeman AD, Cohen JD (2015) Quantitative evaluation of IAA conjugate pools in Arabidopsis thaliana. Planta 241(2):539–548

    CAS  PubMed  Google Scholar 

  53. Yue J, Hu X, Sun H, Yang Y, Huang J (2012) Widespread impact of horizontal gene transfer on plant colonization of land. Nat Commun 3:1152

    PubMed  PubMed Central  Google Scholar 

  54. Zimmer AD, Lang D, Buchta K, Rombauts S, Nishiyama T, Hasebe M, Van de Peer Y, Rensing SA, Reski R (2013) Reannotation and extended community resources for the genome of the non-seed plant Physcomitrella patens provide insights into the evolution of plant gene structures and functions. BMC Genom 14:498–511

    CAS  Google Scholar 

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Acknowledgements

The authors would like to thank Dirk Vanderklein and Scott Kight for their advice and encouragement. We would also like to thank Lisa Campanella for the help in revising this manuscript. The technical help of Adam Parker of MSU and Sabine Rößler, TU Dresden, is gratefully acknowledged. This work was supported by a Margaret and Herman Sokol Fellow Award, #07A. The authors of this article have no conflicts of interest.

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Supplementary Figure S1 Electrophoretic gel analysis of PCR products for specific, non-overlapping genomic regions of PpIAR31, PpIAR32, PpIAR33, and PpIAR34. Lanes 1 & 6: HiLo size marker, Lanes 2 & 4: PCR products for each hydrolase gene, Lanes 3 & 5: 18S PCR control. PCR was performed in duplicate for each reaction set. 2% agarose gel electrophoresed ~35 min at constant 150 volts and stained with ethidium bromide for visualization. The circles on the PpIAR31 panel indicate the lack of expected amplification for this hydrolase gene. (JPG 152 KB)

Supplementary Figure S2 A partial readout of the mRNA expression analysis of PpIAR32, PpIAR33, and PpIAR34, as performed by Lang et al. (2018). Data from Phytozome Web site P. patens v3.3. (JPG 624 KB)

Supplementary Figure S3 Electrophoretic gel analysis of RT-PCR products for specific, non-overlapping mRNA regions of PpIAR32, PpIAR33, and PpIAR34. Lanes 1 & 6: HiLo size marker, Lane 2: PpIAR32 RT-PCR product, Lane 3: PpIAR33, Lane 4: PpIAR34, Lane 5: 18S expression control. 1.5% agarose gel electrophoresed ~30 min at constant 150 volts and stained with ethidium bromide for visualization. (JPG 115 KB)

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Campanella, J.J., Kurdach, S., Skibitski, R. et al. Evidence for the Early Evolutionary Loss of the M20D Auxin Amidohydrolase Family from Mosses and Horizontal Gene Transfer from Soil Bacteria of Cryptic Hydrolase Orthologues to Physcomitrella patens. J Plant Growth Regul 38, 1428–1438 (2019). https://doi.org/10.1007/s00344-019-09945-6

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Keywords

  • Physcomitrella patens
  • Horizontal gene transfer
  • Auxin conjugate regulation
  • Amidohydrolase
  • Cryptic genes
  • Moss evolution