Tandem oleosin genes in a cluster acquired in Brassicaceae created tapetosomes and conferred additive benefit of pollen vigor

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 35, 2013, Pages 14480-14485

  Huang, Chien Yu ^a   Chen, Pei Ying ^b   Huang, Ming Der ^b   Tsou, Chih Hua ^b   Jane, Wann Neng ^b   Huang, Anthony H C ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUTE OF PLANT AND MICROBIAL BIOLOGY   (Taiwan)

Author keywords

Evolutionary appearance of organelle; Tandem gene cluster

Indexed keywords

OLEOSIN; SMALL INTERFERING RNA; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG;

ARABIDOPSIS THALIANA; ARTICLE; CLEOME; CLEOME HASSLERIANA; CONTROLLED STUDY; DNA TRANSFER; GENE CLUSTER; NONHUMAN; PARALOGY; POLLEN; PRIORITY JOURNAL;

EVOLUTIONARY APPEARANCE OF ORGANELLE; TANDEM GENE CLUSTER;

ADAPTATION, PHYSIOLOGICAL; ARABIDOPSIS; BRASSICACEAE; GENES, PLANT; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; MUTATION; PLANT PROTEINS; POLLEN; RNA, MESSENGER;

EID: 84883424728     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1305299110     Document Type: Article

References (32)

1. Birchler JA (2012) Insights from paleogenomic and population studies into the consequences of dosage sensitive gene expression in plants. Curr Opin Plant Biol 15(5): 544-548.
2. Ding Y, Zhou Q, Wang W (2012) Origins of new genes and evolution of their novel functions. Annu Rev Ecol Evol Syst 43:345-363.
3. Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10.
4. Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity (Edinb) 96(1):7-21.
5. Duboule D (2007) The rise and fall of Hox gene clusters. Development 134(14): 2549-2560.
6. Jiang SY, Ma Z, Ramachandran S (2010) Evolutionary history and stress regulation of the lectin superfamily in higher plants. BMC Evol Biol 10:79.
7. Leister D (2004) Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene. Trends Genet 20(3):116-122.
8. Hanada K, Zou C, Lehti-Shiu MD, Shinozaki K, Shiu SH (2008) Importance of lineagespecific expansion of plant tandem duplicates in the adaptive response to environmental stimuli. Plant Physiol 148(2):993-1003.
9. Kim HU, Hsieh K, Ratnayake C, Huang AHC (2002) A novel group of oleosins is present inside the pollen of Arabidopsis. J Biol Chem 277(25):22677-22684.
10. Fiebig A, Kimport R, Preuss D (2004) Comparisons of pollen coat genes across Brassicaceae species reveal rapid evolution by repeat expansion and diversification. Proc Natl Acad Sci USA 101(9):3286-3291.
11. Schein M, Yang Z, Mitchell-Olds T, Schmid KJ (2004) Rapid evolution of a pollenspecific oleosin-like gene family from Arabidopsis thaliana and closely related species. Mol Biol Evol 21(4):659-669.
12. Mayfield JA, Fiebig A, Johnstone SE, Preuss D (2001) Gene families from the Arabidopsis thaliana pollen coat proteome. Science 292(5526):2482-2485.
13. Hsieh K, Huang AHC (2005) Lipid-rich tapetosomes in Brassica tapetum are composed of oleosin-coated oil droplets and vesicles, both assembled in and then detached from the endoplasmic reticulum. Plant J 43(6):889-899.
14. Hsieh K, Huang AHC (2007) Tapetosomes in Brassica tapetum accumulate endoplasmic reticulum-derived flavonoids and alkanes for delivery to the pollen surface. Plant Cell 19(2):582-596.
15. Huang AHC (1992) Oil bodies and oleosins in seeds. Annu Rev Plant Physiol Plant Mol Biol 43:177-200.
16. Hsieh K, Huang AHC (2004) Endoplasmic reticulum, oleosins, and oils in seeds and tapetum cells. Plant Physiol 136(3):3427-3434.
17. Frandsen GI, Mundy J, Tzen JT (2001) Oil bodies and their associated proteins, oleosin and caleosin. Physiol Plant 112(3):301-307.
18. Wu SSH, et al. (1997) Isolation and characterization of neutral-lipid-containing organelles and globuli-filled plastids from Brassica napus tapetum. Proc Natl Acad Sci USA 94(23):12711-12716.
19. Ting JTL, Wu SSH, Ratnayake C, Huang AHC (1998) Constituents of the tapetosomes and elaioplasts in Brassica campestris tapetum and their degradation and retention during microsporogenesis. Plant J 16(5):541-551.
20. Mayfield JA, Preuss D (2000) Rapid initiation of Arabidopsis pollination requires the oleosin-domain protein GRP17. Nat Cell Biol 2(2):128-130.
21. Judd WS, Campbell CS, Kellogg EA, Stevens PF, Donoghue MJ (2002) Brassicales. Plant Systematics (Sinauer Associates, Sunderland, MA), 2nd Ed, pp 402-405.
22. Schranz ME, Mitchell-Olds T (2006) Independent ancient polyploidy events in the sister families Brassicaceae and Cleomaceae. Plant Cell 18(5):1152-1165.
23. Barker MS, Vogel H, Schranz ME (2009) Paleopolyploidy in the Brassicales: Analyses of the Cleome transcriptome elucidate the history of genome duplications in Arabidopsis and other Brassicales. Genome Biol Evol 1:391-399.
24. Newell CA, et al. (2010) Agrobacterium tumefaciens-mediated transformation of Cleome gynandra L., a C(4) dicotyledon that is closely related to Arabidopsis thaliana. J Exp Bot 61(5):1311-1319.
25. Goldberg RB, Beals TP, Sanders PM (1993) Anther development: Basic principles and practical applications. Plant Cell 5(10):1217-1229.
26. Huang MD, Wei FJ, Wu CC, Hsing YIC, Huang AHC (2009) Analyses of advanced rice anther transcriptomes reveal global tapetum secretory functions and potential proteins for lipid exine formation. Plant Physiol 149(2):694-707.
27. Li YB, Suen DF, Huang CY, Kung SY, Huang AHC (2012) The maize tapetum employs diverse mechanisms to synthesize and store proteins and flavonoids and transfer them to the pollen surface. Plant Physiol 158(4):1548-1561.
28. Tantikanjana T, Nasrallah ME, Nasrallah JB (2010) Complex networks of selfincompatibility signaling in the Brassicaceae. Curr Opin Plant Biol 13(5):520-526.
29. Iltis HH, Cochrane TS (2007) Studies in the Cleomaceae V: A new genus and ten new combinations for the flora of North America. Novon 17:447-451.
30. Clough SJ, Bent AF (1998) Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735-743.
31. Li H, Lin YK, Heath RM, Zhu MX, Yang ZB (1999) Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell 11(9):1731-1742.
32. Wang H, Jiang L (2011) Transient expression and analysis of fluorescent reporter proteins in plant pollen tubes. Nat Protoc 6(4):419-426.