TY - JOUR
T1 - Zipcode RNA-binding proteins and membrane trafficking proteins cooperate to transport glutelin mRNAs in rice endosperm[OPEN]
AU - Tian, Li
AU - Doroshenk, Kelly A.
AU - Zhang, Laining
AU - Fukuda, Masako
AU - Washida, Haruhiko
AU - Kumamaru, Toshihiro
AU - Okita, Thomas
N1 - Funding Information:
We thank Ai Nagamine for her help in the construction of BiFC plasmids, and the Franceschi Microscopy and Imaging Center at Washington State University for technical support. This work was supported by the National Science Foundation (grants MCB-1444610 and IOS-1701061), the USDA National Institute of Food and Agriculture (Hatch umbrella project 899–1015621 and project WNP00119), and the Japan Society for the Promotion of Science (to M.F. and T.K.).
Publisher Copyright:
ã 2020 ASPB.
PY - 2020/8
Y1 - 2020/8
N2 - In rice (Oryza sativa) endosperm cells, mRNAs encoding glutelin and prolamine are translated on distinct cortical-endoplasmic reticulum (ER) subdomains (the cisternal-ER and protein body-ER), a process that facilitates targeting of their proteins to different endomembrane compartments. Although the cis- and trans-factors responsible for mRNA localization have been defined over the years, how these mRNAs are transported to the cortical ER has yet to be resolved. Here, we show that the two interacting glutelin zipcode RNA binding proteins (RBPs), RBP-P and RBP-L, form a quaternary complex with the membrane fusion factors N-ethylmaleimide-sensitive factor (NSF) and the small GTPase Rab5a, enabling mRNA transport on endosomes. Direct interaction of RBP-L with Rab5a, between NSF and RBP-P, and between NSF and Rab5a, were established. Biochemical and microscopic analyses confirmed the co-localization of these RBPs with NSF on Rab5a-positive endosomes that carry glutelin mRNAs. Analysis of a loss-of-function rab5a mutant showed that glutelin mRNA and the quaternary complex were mis-targeted to the extracellular paramural body structure formed by aborted endosomal trafficking, further confirming the involvement of endosomal trafficking in glutelin mRNA transport. Overall, these findings demonstrate that mRNA localization in plants co-opts membrane trafficking via the acquisition of new functional binding properties between RBPs and two essential membrane trafficking factors, thus defining an endosomal anchoring mechanism in mRNA localization.
AB - In rice (Oryza sativa) endosperm cells, mRNAs encoding glutelin and prolamine are translated on distinct cortical-endoplasmic reticulum (ER) subdomains (the cisternal-ER and protein body-ER), a process that facilitates targeting of their proteins to different endomembrane compartments. Although the cis- and trans-factors responsible for mRNA localization have been defined over the years, how these mRNAs are transported to the cortical ER has yet to be resolved. Here, we show that the two interacting glutelin zipcode RNA binding proteins (RBPs), RBP-P and RBP-L, form a quaternary complex with the membrane fusion factors N-ethylmaleimide-sensitive factor (NSF) and the small GTPase Rab5a, enabling mRNA transport on endosomes. Direct interaction of RBP-L with Rab5a, between NSF and RBP-P, and between NSF and Rab5a, were established. Biochemical and microscopic analyses confirmed the co-localization of these RBPs with NSF on Rab5a-positive endosomes that carry glutelin mRNAs. Analysis of a loss-of-function rab5a mutant showed that glutelin mRNA and the quaternary complex were mis-targeted to the extracellular paramural body structure formed by aborted endosomal trafficking, further confirming the involvement of endosomal trafficking in glutelin mRNA transport. Overall, these findings demonstrate that mRNA localization in plants co-opts membrane trafficking via the acquisition of new functional binding properties between RBPs and two essential membrane trafficking factors, thus defining an endosomal anchoring mechanism in mRNA localization.
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U2 - 10.1105/tpc.20.00111
DO - 10.1105/tpc.20.00111
M3 - Article
C2 - 32471860
AN - SCOPUS:85089129512
VL - 32
SP - 2566
EP - 2581
JO - Plant Cell
JF - Plant Cell
SN - 1040-4651
IS - 8
ER -