TY - JOUR
T1 - Characterization of ancestral myosin XI from Marchantia polymorpha by heterologous expression in Arabidopsis thaliana
AU - Duan, Zhongrui
AU - Tanaka, Misato
AU - Kanazawa, Takehiko
AU - Haraguchi, Takeshi
AU - Takyu, Akiko
AU - Era, Atsuko
AU - Ueda, Takashi
AU - Ito, Kohji
AU - Tominaga, Motoki
N1 - Funding Information:
We thank Kengo Okazaki and Kae Yoshino for their technical assistance with the experiments. We thank Dr V. V. Dolja of Oregon State University for providing the seeds for the xi-1 xi-2 xi-k xi-i mutants. We also thank Dr Takayuki Kohchi, Dr Ryuichi Nishihama of Kyoto University, Dr Katsuyuki T. Yamato of Kindai University and Dr Kimitsune Ishizaki of Kobe University for sharing materials from their Marchantia polymorpha research. This work was supported by grants from the Japan Society for the Promotion of Science KAKENHI (no. 20001009, no. 23770060 and no. 25221103 to MT; 24114003, 15H04382, 17K19412, 18H02470, 19H05670 and 19H05675 to TU; 17H07333 and 18K14738 to TK; and no. 24658002, no. 26440131 and no. 15H01309 to KI) and from the Japan Science and Technology Agency, ALCA (JPMJAL1401 to KI and MT) and from the NIBB Collaborative Research Program (16-346 to KI).
Funding Information:
This work was supported by grants from the Japan Society for the Promotion of Science KAKENHI (no. 20001009, no. 23770060 and no. 25221103 to MT; 24114003, 15H04382, 17K19412, 18H02470, 19H05670 and 19H05675 to TU; 17H07333 and 18K14738 to TK; and no. 24658002, no. 26440131 and no. 15H01309 to KI) and from the Japan Science and Technology Agency, ALCA (JPMJAL1401 to KI and MT) and from the NIBB Collaborative Research Program (16‐346 to KI).
Publisher Copyright:
© 2020 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd
PY - 2020/10/1
Y1 - 2020/10/1
N2 - Previous studies have revealed duplications and diversification of myosin XI genes between angiosperms and bryophytes; however, the functional differentiation and conservation of myosin XI between them remain unclear. Here, we identified a single myosin XI gene from the liverwort Marchantia polymorpha (Mp). The molecular properties of Mp myosin XI are similar to those of Arabidopsis myosin XIs responsible for cytoplasmic streaming, suggesting that the motor function of myosin XI is able to generate cytoplasmic streaming. In cultured Arabidopsis cells, transiently expressed green fluorescent protein (GFP)-fused Mp myosin XI was observed as some intracellular structures moving along the F-actin. These intracellular structures were co-localized with motile endoplasmic reticulum (ER) strands, suggesting that Mp myosin XI binds to the ER and generates intracellular transport in Arabidopsis cells. The tail domain of Mp myosin XI was co-localized with that of Arabidopsis myosin XI-2 and XI-K, suggesting that all these myosin XIs bind to common cargoes. Furthermore, expression of GFP-fused Mp myosin XI rescued the defects of growth, cytoplasmic streaming and actin organization in Arabidopsis multiple myosin XI knockout mutants. The heterologous expression experiments demonstrated the cellular and physiological competence of Mp myosin XI in Arabidopsis. However, the average velocity of organelle transport in Marchantia rhizoids was 0.04 ± 0.01 μm s−1, which is approximately one-hundredth of that in Arabidopsis cells. Taken together, our results suggest that the molecular properties of myosin XI are conserved, but myosin XI-driven intracellular transport in vivo would be differentiated from bryophytes to angiosperms.
AB - Previous studies have revealed duplications and diversification of myosin XI genes between angiosperms and bryophytes; however, the functional differentiation and conservation of myosin XI between them remain unclear. Here, we identified a single myosin XI gene from the liverwort Marchantia polymorpha (Mp). The molecular properties of Mp myosin XI are similar to those of Arabidopsis myosin XIs responsible for cytoplasmic streaming, suggesting that the motor function of myosin XI is able to generate cytoplasmic streaming. In cultured Arabidopsis cells, transiently expressed green fluorescent protein (GFP)-fused Mp myosin XI was observed as some intracellular structures moving along the F-actin. These intracellular structures were co-localized with motile endoplasmic reticulum (ER) strands, suggesting that Mp myosin XI binds to the ER and generates intracellular transport in Arabidopsis cells. The tail domain of Mp myosin XI was co-localized with that of Arabidopsis myosin XI-2 and XI-K, suggesting that all these myosin XIs bind to common cargoes. Furthermore, expression of GFP-fused Mp myosin XI rescued the defects of growth, cytoplasmic streaming and actin organization in Arabidopsis multiple myosin XI knockout mutants. The heterologous expression experiments demonstrated the cellular and physiological competence of Mp myosin XI in Arabidopsis. However, the average velocity of organelle transport in Marchantia rhizoids was 0.04 ± 0.01 μm s−1, which is approximately one-hundredth of that in Arabidopsis cells. Taken together, our results suggest that the molecular properties of myosin XI are conserved, but myosin XI-driven intracellular transport in vivo would be differentiated from bryophytes to angiosperms.
KW - Marchantia polymorpha
KW - cytoplasmic streaming
KW - heterologous expression
KW - myosin XI
UR - http://www.scopus.com/inward/record.url?scp=85089017063&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85089017063&partnerID=8YFLogxK
U2 - 10.1111/tpj.14937
DO - 10.1111/tpj.14937
M3 - Article
C2 - 32717107
AN - SCOPUS:85089017063
SN - 0960-7412
VL - 104
SP - 460
EP - 473
JO - Plant Journal
JF - Plant Journal
IS - 2
ER -