The speed of mitochondrial movement is regulated by the cytoskeleton and myosin in Picea wilsonii pollen tubes

Planta

Volumn 231, Issue 4, 2010, Pages 779-791

  Zheng, Maozhong ^a,b   Wang, Qinli ^a   Teng, Yan ^c   Wang, Xiaohua ^a,b   Wang, Feng ^a,b   Chen, Tong ^a   Šamaj, Jozef ^d,e   Lin, Jinxing ^a   Logan, David C ^f  

^a INSTITUTE OF BOTANY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c INSTITUTE OF BIOPHYSICS   (China)

^d UNIVERSITY OF BONN   (Germany)

^e PALACKÝ UNIVERSITY   (Czech Republic)

^f UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Actin filaments; Microtubules; Mitochondrial movement; Myosin; Trajectory; Velocity

Indexed keywords

2,3 BUTANEDIONE; DIACETYL OXIME; DRUG DERIVATIVE; ENZYME INHIBITOR; FUSED HETEROCYCLIC RINGS; LATRUNCULIN B; MYOSIN; PACLITAXEL; THIAZOLIDINE DERIVATIVE;

ARTICLE; CYTOSKELETON; DRUG ANTAGONISM; DRUG EFFECT; METABOLISM; MICROTUBULE; MITOCHONDRION; POLLEN TUBE; SPRUCE;

BICYCLO COMPOUNDS, HETEROCYCLIC; CYTOSKELETON; DIACETYL; ENZYME INHIBITORS; MICROTUBULES; MITOCHONDRIA; MYOSINS; PACLITAXEL; PICEA; POLLEN TUBE; THIAZOLIDINES;

PICEA; PICEA WILSONII;

EID: 77950547934     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-009-1086-0     Document Type: Article

References (39)

1. Avisar D, Prokhnevsky AI, Makarova KS, Koonin EV, Dolja VV (2008) Myosin XI-K is required for rapid trafficking of Golgi stacks, peroxisomes, and mitochondria in leaf cells of Nicotiana benthamiana. Plant Physiol 146: 1098-1108.
2. Basu R, Chang F (2007) Shaping the actin cytoskeleton using microtubule tips. Curr Opin Cell Biol 19: 88-94.
3. Bereiter-Hahn J (1990) Behavior of mitochondria in the living cell. Int Rev Cytol 122: 1-63.
4. Bove J, Vaillancourt B, Kroeger J, Hepler PK, Wiseman PW, Geitmann A (2008) Magnitude and direction of vesicle dynamics in growing pollen tubes using spatiotemporal image correlation spectroscopy and fluorescence recovery after photobleaching. Plant Physiol 147: 1646-1658.
5. Chen T, Teng N, Wu X, Wang Y, Tang W, Samaj J, Baluska F, Lin J (2007) Disruption of actin filaments by latrunculin b affects cell wall construction in Picea meyeri pollen tube by disturbing vesicle trafficking. Plant Cell Physiol 48: 19-30.
6. Cheung AY, Wu HM (2004) Overexpression of an Arabidopsis formin stimulates supernumerary actin cable formation from pollen tube cell membrane. Plant Cell 16: 257-269.
7. Cheung AY, Wu HM (2008) Structural and signaling networks for the polar cell growth machinery in pollen tubes. Annu Rev Plant Biol 59: 547-572.
8. de Win AHN, Pierson ES, Derksen J (1999) Rational analyses of organelle trajectories in tobacco pollen tubes reveal characteristics of the actomyosin cytoskeleton. Biophys J 76: 1648-1658.
9. Demaurex N, Distelhorst C (2003) Cell biology. Apoptosis-the calcium connection. Science 300: 65-67.
10. Doniwa Y, Arimura S, Tsutsumi N (2007) Mitochondria use actin filaments as rails for fast translocation in Arabidopsis and tobacco cells. Plant Biotechnol 24: 441-447.
11. Dramsi S, Cossart P (1998) Intracellular pathogens and the actin cytoskeleton. Annu Rev Cell Dev Biol 14: 137-166.
12. Fehrenbacher KL, Yang HC, Gay AC, Huckaba TM, Pon LA (2004) Live cell imaging of mitochondrial movement along actin cables in budding yeast. Curr Biol 14: 1996-2004.
13. Hao H, Li Y, Hu Y, Lin J (2005) Inhibition of rna and protein synthesis in pollen tube development of Pinus bungeana by actinomycin D and cycloheximide. New Phytol 165: 721-729.
14. Ligon LA, Steward O (2000) Role of microtubules and actin filaments in the movement of mitochondria in the axons and dendrites of cultured hippocampal neurons. J Comp Neurol 427: 351-361.
15. Logan DC (2006) The mitochondrial compartment. J Exp Bot 57: 1225-1243.
16. Logan DC, Leaver CJ (2000) Mitochondria-targeted gfp highlights the heterogeneity of mitochondrial shape, size and movement within living plant cells. J Exp Bot 51: 865-871.
17. Miller KE, Sheetz MP (2006) Direct evidence for coherent low velocity axonal transport of mitochondria. J Cell Biol 173: 373-381.
18. Minin AA, Kulik AV, Gyoeva FK, Li Y, Goshima G, Gelfand VI (2006) Regulation of mitochondria distribution by rhoa and formins. J Cell Sci 119: 659-670.
19. Olyslaegers G, Verbelen JP (1998) Improved staining of F-actin and co-localization of mitochondria in plant cells. J Microsc 192: 73-77.
20. Peremyslov VV, Prokhnevsky AI, Avisar D, Dolja VV (2008) Two class XI myosins function in organelle trafficking and root hair development in Arabidopsis. Plant Physiol 146: 1109-1116.
21. Prokhnevsky AI, Peremyslov VV, Dolja VV (2008) Overlapping functions of the four class XI myosins in Arabidopsis growth, root hair elongation, and organelle motility. Proc Natl Acad Sci USA 105: 19744-19749.
22. Reddy ASN, Day IS (2001) Analysis of the myosins encoded in the recently completed Arabidopsis thaliana genome sequence. Genome Biol 2: 1-18.
23. 2+ liaison. Sci STKE 2004: re1.
24. Semenova L, Burakov A, Berardone N, Zaliapin L, Slepchenko B, Svitkina T, Kashina A, Rodionov V (2008) Actin dynamics is essential for myosin-based transport of membrane organelles. Curr Biol 18: 1-6.
25. Sheahan MB, McCurdy DW, Rose RJ (2005) Mitochondria as a connected population: ensuring continuity of the mitochondrial genome during plant cell dedifferentiation through massive mitochondrial fusion. Plant J 44: 744-755.
26. Sheng X, Hu Z, Lü H, Wang X, Baluška F, Šamaj J, Lin J (2006) Roles of the ubiquitin/proteasome pathway in pollen tube growth with emphasis on MG132-induced alterations in ultrastructure, cytoskeleton, and cell wall components. Plant Physiol 141: 1578-1590.
27. Sieberer BJ, Ketelaar T, Esseling JJ, Emons AM (2005) Microtubules guide root hair tip growth. New Phytol 167: 711-719.
28. Sparkes IA, Teanby NA, Hawes C (2008) Truncated myosin XI tail fusions inhibit peroxisome, Golgi, and mitochondrial movement in tobacco leaf epidermal cells: a genetic tool for the next generation. J Exp Bot 59: 2499-2512.
29. Staiger CJ, Sheahan MB, Khurana P, Wang X, McCurdy DW, Blanchoin L (2009) Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array. J Cell Biol 184: 269-280.
30. Taraska JW, Almers W (2004) Bilayers merge even when exocytosis is transient. Proc Natl Acad Sci USA 101: 8780-8785.
31. Tominaga M, Morita K, Sonobe S, Yokota E, Shimmen T (1997) Microtubules regulate the organization of actin filaments at the cortical region in root hair cells of Hydrocharis. Protoplasma 199: 83-92.
32. Tominaga M, Kojima H, Yokota E, Orii H, Nakamori R, Katayama E, Anson M, Shimmen T, Oiwa K (2003) Higher plant myosin xi moves processively on actin with 35 nm steps at high velocity. EMBO J 22: 1263-1272.
33. Trinczek B, Ebneth A, Mandelkow EM, Mandelkow E (1999) Tau regulates the attachment/detachment but not the speed of motors in microtubule-dependent transport of single vesicles and organelles. J Cell Sci 112: 2355-2367.
34. Tsuboi T, Zhao C, Terakawa S, Rutter GA (2000) Simultaneous evanescent wave imaging of insulin vesicle membrane and cargo during a single exocytotic event. Curr Biol 10: 1307-1310.
35. van Gestel K, Kohler RH, Verbelen JP (2002) Plant mitochondria move on f-actin, but their positioning in the cortical cytoplasm depends on both f-actin and microtubules. J Exp Bot 53: 659-667.
36. Wang Q, Kong L, Hao H, Wang X, Lin J, Samaj J, Baluska F (2005) Effects of brefeldin a on pollen germination and tube growth. Antagonistic effects on endocytosis and secretion. Plant Physiol 139: 1692-1703.
37. Wang X, Teng Y, Wang Q, Li X, Sheng X, Zheng M, Samaj J, Baluska F, Lin J (2006) Imaging of dynamic secretory vesicles in living pollen tubes of Picea meyeri using evanescent wave microscopy. Plant Physiol 141: 1591-1603.
38. Yi M, Weaver D, Hajnoczky G (2004) Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit. J Cell Biol 167: 661-672.
39. Zheng M, Beck M, Müller J, Chen T, Wang X, Wang F, Wang Q, Wang Y, Baluska F, Logan DC, Samaj J, Lin J (2009) Actin turnover is required for myosin-dependent mitochondrial movements in Arabidopsis root hairs. PLoS One 4: e5961.