TY - JOUR

T1 - Initiation of cytosolic plant purine nucleotide catabolism involves a monospecific xanthosine monophosphate phosphatase

AU - Heinemann, Katharina J.

AU - Yang, Sun-Young

AU - Straube, Henryk

AU - Medina-Escobar, Nieves

AU - Varbanova-Herde, Marina

AU - Herde, Marco

AU - Rhee, Sangkee

AU - Witte, Claus-Peter

N1 - Funding Information: We thank André Specht and Hildegard Thölke for technical assistance and Anting Zhu for generating the clones X130, X131, and X144; Christel Schmiechen for generating the clone H453 and Mingjia Chen for generating the vector V108 as well as Ludwig Hothorn for advice concerning the statistical analysis. This work was supported by the Deutsche Forschungsgemeinschaft (DFG) grants WI3411/8-1, INST 187/741-1 FUGG, and GRK1798 “Signaling at the Plant-Soil Interface” for C.-P.W., and by the National Research Foundation of Korea (NRF) grant 2020R1A4A1018890 by the Korea government (MSIT) for S.R.

PY - 2021/12

Y1 - 2021/12

N2 - In plants, guanosine monophosphate (GMP) is synthesized from adenosine monophosphate via inosine monophosphate and xanthosine monophosphate (XMP) in the cytosol. It has been shown recently that the catabolic route for adenylate-derived nucleotides bifurcates at XMP from this biosynthetic route. Dephosphorylation of XMP and GMP by as yet unknown phosphatases can initiate cytosolic purine nucleotide catabolism. Here we show that Arabidopsis thaliana possesses a highly XMP-specific phosphatase (XMPP) which is conserved in vascular plants. We demonstrate that XMPP catalyzes the irreversible entry reaction of adenylate-derived nucleotides into purine nucleotide catabolism in vivo, whereas the guanylates enter catabolism via an unidentified GMP phosphatase and guanosine deaminase which are important to maintain purine nucleotide homeostasis. We also present a crystal structure and mutational analysis of XMPP providing a rationale for its exceptionally high substrate specificity, which is likely required for the efficient catalysis of the very small XMP pool in vivo.

AB - In plants, guanosine monophosphate (GMP) is synthesized from adenosine monophosphate via inosine monophosphate and xanthosine monophosphate (XMP) in the cytosol. It has been shown recently that the catabolic route for adenylate-derived nucleotides bifurcates at XMP from this biosynthetic route. Dephosphorylation of XMP and GMP by as yet unknown phosphatases can initiate cytosolic purine nucleotide catabolism. Here we show that Arabidopsis thaliana possesses a highly XMP-specific phosphatase (XMPP) which is conserved in vascular plants. We demonstrate that XMPP catalyzes the irreversible entry reaction of adenylate-derived nucleotides into purine nucleotide catabolism in vivo, whereas the guanylates enter catabolism via an unidentified GMP phosphatase and guanosine deaminase which are important to maintain purine nucleotide homeostasis. We also present a crystal structure and mutational analysis of XMPP providing a rationale for its exceptionally high substrate specificity, which is likely required for the efficient catalysis of the very small XMP pool in vivo.

UR - http://www.scopus.com/inward/record.url?scp=85119834611&partnerID=8YFLogxK

U2 - 10.1038/s41467-021-27152-4

DO - 10.1038/s41467-021-27152-4

M3 - Article

VL - 12

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

IS - 1

M1 - 6846

ER -