Biochemical Principles and Functional Aspects of Pipecolic Acid Biosynthesis in Plant Immunity.
The nonprotein amino acid pipecolic acid (Pip) regulates plant systemic acquired resistance and basal immunity to bacterial pathogen infection. In Arabidopsis (Arabidopsis thaliana), the lysine (Lys) aminotransferase AGD2-LIKE DEFENSE RESPONSE PROTEIN1 (ALD1) mediates the pathogen-induced accumulation of Pip in inoculated and distal leaf tissue. Here, we show that ALD1 transfers the α-amino group of l-Lys to acceptor oxoacids. Combined mass spectrometric and infrared spectroscopic analyses of in vitro assays and plant extracts indicate that the final product of the ALD1-catalyzed reaction is enaminic 2,3-dehydropipecolic acid (DP), whose formation involves consecutive transamination, cyclization, and isomerization steps. Besides l-Lys, recombinant ALD1 transaminates l-methionine, l-leucine, diaminopimelate, and several other amino acids to generate oxoacids or derived products in vitro. However, detailed in planta analyses suggest that the biosynthesis of 2,3-DP from l-Lys is the major in vivo function of ALD1. Sinceald1mutant plants are able to convert exogenous 2,3-DP into Pip, their Pip deficiency relies on the inability to form the 2,3-DP intermediate. The Arabidopsis reductase ornithine cyclodeaminase/μ-crystallin, alias SYSTEMIC ACQUIRED RESISTANCE-DEFICIENT4 (SARD4), converts ALD1-generated 2,3-DP into Pip in vitro. SARD4 significantly contributes to the production of Pip in pathogen-inoculated leaves but is not the exclusive reducing enzyme involved in Pip biosynthesis. FunctionalSARD4is required for proper basal immunity to the bacterial pathogenPseudomonas syringaeAlthoughSARD4knockout plants show greatly reduced accumulation of Pip in leaves distal toP. syringaeinoculation, they display a considerable systemic acquired resistance response. This suggests a triggering function of locally accumulating Pip for systemic resistance induction.
Institute for Molecular Ecophysiology of Plants (M.H., D.K., F.B., Z.A.-R., N.S., S.Schr., T.Z., S.Schu., V.R.-D., J.Z.) and Cluster of Excellence on Plant Sciences (Z.A.-R., S.Schu., J.Z.), Heinrich Heine University, D-40225 Duesseldorf, Germany.
Michael
http://orcid.org/0000-0003-4828-958X
M
Hartmann
Institute for Molecular Ecophysiology of Plants (M.H., D.K., F.B., Z.A.-R., N.S., S.Schr., T.Z., S.Schu., V.R.-D., J.Z.) and Cluster of Excellence on Plant Sciences (Z.A.-R., S.Schu., J.Z.), Heinrich Heine University, D-40225 Duesseldorf, Germany.
Denis
D
Kim
Institute for Molecular Ecophysiology of Plants (M.H., D.K., F.B., Z.A.-R., N.S., S.Schr., T.Z., S.Schu., V.R.-D., J.Z.) and Cluster of Excellence on Plant Sciences (Z.A.-R., S.Schu., J.Z.), Heinrich Heine University, D-40225 Duesseldorf, Germany.
Friederike
http://orcid.org/0000-0003-3457-2034
F
Bernsdorff
Institute for Molecular Ecophysiology of Plants (M.H., D.K., F.B., Z.A.-R., N.S., S.Schr., T.Z., S.Schu., V.R.-D., J.Z.) and Cluster of Excellence on Plant Sciences (Z.A.-R., S.Schu., J.Z.), Heinrich Heine University, D-40225 Duesseldorf, Germany.
Ziba
http://orcid.org/0000-0003-4884-8302
Z
Ajami-Rashidi
Institute for Molecular Ecophysiology of Plants (M.H., D.K., F.B., Z.A.-R., N.S., S.Schr., T.Z., S.Schu., V.R.-D., J.Z.) and Cluster of Excellence on Plant Sciences (Z.A.-R., S.Schu., J.Z.), Heinrich Heine University, D-40225 Duesseldorf, Germany.
Nicola
http://orcid.org/0000-0002-9532-8687
N
Scholten
Institute for Molecular Ecophysiology of Plants (M.H., D.K., F.B., Z.A.-R., N.S., S.Schr., T.Z., S.Schu., V.R.-D., J.Z.) and Cluster of Excellence on Plant Sciences (Z.A.-R., S.Schu., J.Z.), Heinrich Heine University, D-40225 Duesseldorf, Germany.
Stefan
S
Schreiber
Institute for Molecular Ecophysiology of Plants (M.H., D.K., F.B., Z.A.-R., N.S., S.Schr., T.Z., S.Schu., V.R.-D., J.Z.) and Cluster of Excellence on Plant Sciences (Z.A.-R., S.Schu., J.Z.), Heinrich Heine University, D-40225 Duesseldorf, Germany.
Tatyana
T
Zeier
Institute for Molecular Ecophysiology of Plants (M.H., D.K., F.B., Z.A.-R., N.S., S.Schr., T.Z., S.Schu., V.R.-D., J.Z.) and Cluster of Excellence on Plant Sciences (Z.A.-R., S.Schu., J.Z.), Heinrich Heine University, D-40225 Duesseldorf, Germany.
Stefan
S
Schuck
Institute for Molecular Ecophysiology of Plants (M.H., D.K., F.B., Z.A.-R., N.S., S.Schr., T.Z., S.Schu., V.R.-D., J.Z.) and Cluster of Excellence on Plant Sciences (Z.A.-R., S.Schu., J.Z.), Heinrich Heine University, D-40225 Duesseldorf, Germany.
Vanessa
V
Reichel-Deland
Institute for Molecular Ecophysiology of Plants (M.H., D.K., F.B., Z.A.-R., N.S., S.Schr., T.Z., S.Schu., V.R.-D., J.Z.) and Cluster of Excellence on Plant Sciences (Z.A.-R., S.Schu., J.Z.), Heinrich Heine University, D-40225 Duesseldorf, Germany juergen.zeier@uni-duesseldorf.de.
Jürgen
http://orcid.org/0000-0002-8703-5403
J
Zeier
D017360:Arabidopsis / Q000235:genetics / Q000276:immunology* / Q000382:microbiology; D029681:Arabidopsis Proteins / Q000235:genetics / Q000276:immunology / Q000378:metabolism; D054884:Host-Pathogen Interactions / Q000276:immunology; D007651:Keto Acids / Q000276:immunology / Q000378:metabolism; D007930:Leucine / Q000276:immunology / Q000378:metabolism; D008239:Lysine / Q000276:immunology / Q000378:metabolism; D008715:Methionine / Q000276:immunology / Q000378:metabolism; D010875:Pipecolic Acids / Q000276:immunology* / Q000378:metabolism; D010935:Plant Diseases / Q000235:genetics / Q000276:immunology* / Q000382:microbiology; D057865:Plant Immunity; D044224:Pseudomonas syringae / Q000276:immunology* / Q000502:physiology; D000637:Transaminases / Q000235:genetics / Q000276:immunology / Q000378:metabolism
D029681:Arabidopsis Proteins; D007651:Keto Acids; D010875:Pipecolic Acids; D008715:Methionine; C487185:AGD2-LIKE DEFENSE RESPONSE PROTEIN1, Arabidopsis; D000637:Transaminases; D007930:Leucine; D008239:Lysine