PYK10 myrosinase reveals a functional coordination between endoplasmic reticulum bodies and glucosinolates in Arabidopsis thaliana.
The endoplasmic reticulum body (ER body) is an organelle derived from the ER that occurs in only three families of the order Brassicales and is suggested to be involved in plant defense. ER bodies in Arabidopsis thaliana contain large amounts of β-glucosidases, but the physiological functions of ER bodies and these enzymes remain largely unclear. Here we show that PYK10, the most abundant β-glucosidase in A. thaliana root ER bodies, hydrolyzes indole glucosinolates (IGs) in addition to the previously reported in vitro substrate scopolin. We found a striking co-expression between ER body-related genes (including PYK10), glucosinolate biosynthetic genes and the genes for so-called specifier proteins affecting the terminal products of myrosinase-mediated glucosinolate metabolism, indicating that these systems have been integrated into a common transcriptional network. Consistent with this, comparative metabolite profiling utilizing a number of A. thaliana relatives within Brassicaceae identified a clear phylogenetic co-occurrence between ER bodies and IGs, but not between ER bodies and scopolin. Collectively, our findings suggest a functional link between ER bodies and glucosinolate metabolism in planta. In addition, in silico three-dimensional modeling, combined with phylogenomic analysis, suggests that PYK10 represents a clade of 16 myrosinases that arose independently from the other well-documented class of six thioglucoside glucohydrolases. These findings provide deeper insights into how glucosinolates are metabolized in cruciferous plants and reveal variation of the myrosinase-glucosinolate system within individual plants.
Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, D-50829, Köln, Germany.|Cluster of Excellence on Plant Sciences (CEPLAS), Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, D-50829, Köln, Germany.|Department of Botany, Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto, 606-8502, Japan.
Ryohei T
RT
Nakano
Institute of Bioorganic Chemistry, Polish Academy of Sciences, Noskowskiego 12/14, 61-704, Poznań, Poland.
Mariola
M
Piślewska-Bednarek
Department of Cell Biology, National Institute of Basic Biology, Okazaki, 444-8585, Japan.
Kenji
0000-0003-4872-3729
K
Yamada
Department of Plant and Microbial Biology, University of California, Berkeley, CA, 94720, USA.
Patrick P
PP
Edger
Department of Botany, Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto, 606-8502, Japan.
Mado
M
Miyahara
Department of Cell Biology, National Institute of Basic Biology, Okazaki, 444-8585, Japan.
Maki
M
Kondo
Department of Stress and Developmental Biology, Leibniz Institute of Plant Biochemistry, D-06120, Halle (Saale), Germany.
Christoph
C
Böttcher
Ishikawa Prefectural University, Nonoichi, Ishikawa, 834-1213, Japan.
Masashi
M
Mori
Department of Cell Biology, National Institute of Basic Biology, Okazaki, 444-8585, Japan.
Mikio
M
Nishimura
Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, D-50829, Köln, Germany.|Cluster of Excellence on Plant Sciences (CEPLAS), Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, D-50829, Köln, Germany.
Paul
P
Schulze-Lefert
Department of Botany, Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto, 606-8502, Japan.
Ikuko
I
Hara-Nishimura
Institute of Bioorganic Chemistry, Polish Academy of Sciences, Noskowskiego 12/14, 61-704, Poznań, Poland.
Paweł
0000-0002-3064-7775
P
Bednarek
D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D004721:Endoplasmic Reticulum / Q000378:metabolism*; D019143:Evolution, Molecular; D018506:Gene Expression Regulation, Plant; D005961:Glucosinolates / Q000378:metabolism*; D007211:Indoles / Q000378:metabolism; D010802:Phylogeny; D001617:beta-Glucosidase / Q000235:genetics / Q000378:metabolism*
D029681:Arabidopsis Proteins; D005961:Glucosinolates; D007211:Indoles; C048308:glucobrassicin; C473372:PYK10 protein, Arabidopsis; D001617:beta-Glucosidase

Arabidopsis thaliana
; Brassicaceae; ER body; co-expression; glucosinolate; molecular phylogeny; myrosinase