Abstract
Although a large number of genes encoding the WD40 motif have been identified as being involved in various developmental processes in Arabidopsis, little is known about the function of these genes in rice (Oryza sativa). Here, we report the cloning and functional characterization of a novel rice gene OsLIS-L1 (Lissencephaly type-1-like 1), which is required for normal fertility and the first internode elongation. OsLIS-L1 encodes a lissencephaly type-1-like protein containing the WD40 motif that is required for brain development in human. SMART algorithm analysis indicated that OsLIS-L1 contains a LIS1 homology (LisH) domain, a C terminus to LisH (CTLH) domain, a five WD40-repeat domain in the middle, and a domain with four WD40 repeats which is homologous to the β subunit of trimeric G-proteins (Gβ). OsLIS-L1 transcript is relatively highly abundant in stem and panicle and has a dynamic expression pattern at different panicle developmental stages. Two independent alleles, designated oslis-l1-1 and oslis-l1-2, exhibited similar abnormal developmental phenotypes, including semi-dwarf, shorter panicle length, and reduced male fertility. Cytological examination confirmed that OsLIS-L1 does not affect the meiosis in pollen mother cells. Compared with wild type, the oslis-l1 mutant had abnormal male gametophyte formation, but anther cell wall and pollen wall development were not affected. Histological analysis revealed that OsLIS-L1 regulates the cell proliferation in the first internode under the panicle. Our results indicate that OsLIS-L1 plays an important role in male gametophyte formation and the first internode elongation in rice.
Similar content being viewed by others
References
Armstrong SJ, Caryl AP, Jones GH, Franklin FC (2002) Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J Cell Sci 115:3645–3655
Chang Y, Gong L, Yuan W, Li X, Chen G, Zhang Q, Wu C (2009) Replication protein A (RPA1a) is required for meiotic and somatic DNA repair but is dispensable for DNA replication and homologous recombination in rice. Plant Physiol 151:2162–2173
Chen R, Zhao X, Shao Z, Wei Z, Wang Y, Zhu L, Zhao J, Sun M, He R, He G (2007) Rice UDP-glucose pyrophosphorylase1 is essential for pollen callose deposition and its cosuppression results in a new type of thermosensitive genic male sterility. Plant Cell 19:847–861
Chu Z, Yuan M, Yao J, Ge X, Yuan B, Xu C, Li X, Fu B, Li Z, Bennetzen JL, Zhang Q, Wang S (2006) Promoter mutations of an essential gene for pollen development result in disease resistance in rice. Genes Dev 20:1250–1255
Emes RD, Ponting CP (2001) A new sequence motif linking lissencephaly, Treacher Collins and oral-facial-digital type 1 syndromes, microtubule dynamics and cell migration. Hum Mol Genet 10:2813–2820
Franks RG, Wang C, Levin JZ, Liu Z (2002) SEUSS, a member of a novel family of plant regulatory proteins, represses floral homeotic gene expression with LEUNIG. Development 129:253–263
Han MJ, Jung KH, Yi G, Lee DY, An G (2006) Rice Immature Pollen 1 (RIP1) is a regulator of late pollen development. Plant Cell Physiol 47:1457–1472
Hoecker U, Tepperman JM, Quail PH (1999) SPA1, a WD-repeat protein specific to phytochrome A signal transduction. Science 284:496–499
Holm M, Ma LG, Qu LJ, Deng XW (2002) Two interacting bZIP proteins are direct targets of COP1-mediated control of light-dependent gene expression in Arabidopsis. Genes Dev 16:1247–1259
Hu L, Liang W, Yin C, Cui X, Zong J, Wang X, Hu J, Zhang D (2011) Rice MADS3 regulates ROS homeostasis during late anther development. Plant Cell 23:515–533
Huang J, Wang MM, Bao YM, Sun SJ, Pan LJ, Zhang HS (2008) SRWD: a novel WD40 protein subfamily regulated by salt stress in rice (Oryza sativa L.). Gene 424:71–79
Jeon JS, Lee S, Jung KH, Jun SH, Jeong DH, Lee J, Kim C, Jang S, Yang K, Nam J, An K, Han MJ, Sung RJ, Choi HS, Yu JH, Choi JH, Cho SY, Cha SS, Kim SI, An G (2000) T-DNA insertional mutagenesis for functional genomics in rice. Plant J 22:561–570
Jeong DH, An S, Park S, Kang HG, Park GG, Kim SR, Sim J, Kim YO, Kim MK, Kim J, Shin M, Jung M, An G (2006) Generation of a flanking sequence-tag database for activation-tagging lines in japonica rice. Plant J 45:123–132
Jung KH, Han MJ, Lee YS, Kim YW, Hwang I, Kim MJ, Kim YK, Nahm BH, An G (2005) Rice Undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 17:2705–2722
Jung KH, Han MJ, Lee DY, Lee YS, Schreiber L, Franke R, Faust A, Yephremov A, Saedler H, Kim YW, Hwang I, An G (2006) Wax-deficient anther1 is involved in cuticle and wax production in rice anther walls and is required for pollen development. Plant Cell 18:3015–3032
Kaya H, Shibahara KI, Taoka KI, Iwabuchi M, Stillman B, Araki T (2001) FASCIATA genes for chromatin assembly factor-1 in Arabidopsis maintain the cellular organization of apical meristems. Cell 104:131–142
Kim MH, Cooper DR, Oleksy A, Devedjiev Y, Derewenda U, Reiner O, Otlewski J, Derewenda ZS (2004) The structure of the N-terminal domain of the product of the lissencephaly gene Lis1 and its functional implications. Structure 12:987–998
Kumar M, Basha PO, Puri A, Rajpurohit D, Randhawa GS, Sharma TR, Dhaliwal HS (2010) A candidate gene OsAPC6 of anaphase-promoting complex of rice identified through T-DNA insertion. Funct Integr Genomics 10:349–358
Lee JH, Terzaghi W, Gusmaroli G, Charron JB, Yoon HJ, Chen H, He YJ, Xiong Y, Deng XW (2008) Characterization of Arabidopsis and rice DWD proteins and their roles as substrate receptors for CUL4-RING E3 ubiquitin ligases. Plant Cell 20:152–167
Li N, Zhang DS, Liu HS, Yin CS, Li XX, Liang WQ, Yuan Z, Xu B, Chu HW, Wang J, Wen TQ, Huang H, Luo D, Ma H, Zhang DB (2006) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18:2999–3014
Li H, He Z, Lu G, Lee SC, Alonso J, Ecker JR, Luan S (2007) A WD40 domain cyclophilin interacts with histone H3 and functions in gene repression and organogenesis in Arabidopsis. Plant Cell 19:2403–2416
Li H, Pinot F, Sauveplane V, Werck-Reichhart D, Diehl P, Schreiber L, Franke R, Zhang P, Chen L, Gao Y, Liang W, Zhang D (2010) Cytochrome P450 family member CYP704B2 catalyzes the {omega}-hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. Plant Cell 22:173–190
Li H, Yuan Z, Vizcay-Barrena G, Yang C, Liang W, Zong J, Wilson ZA, Zhang D (2011a) PERSISTENT TAPETAL CELL1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiol 156:615–630
Li X, Gao X, Wei Y, Deng L, Ouyang Y, Chen G, Li X, Zhang Q, Wu C (2011b) Rice APOPTOSIS INHIBITOR5 coupled with two DEAD-Box adenosine 5′-triphosphate-dependent RNA helicases regulates tapetum degeneration. Plant Cell 23:1416–1434
Liu Z, Meyerowitz EM (1995) LEUNIG regulates AGAMOUS expression in Arabidopsis flowers. Development 121:975–991
Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56:393–434
McNellis TW, von Arnim AG, Araki T, Komeda Y, Misera S, Deng XW (1994) Genetic and molecular analysis of an allelic series of cop1 mutants suggests functional roles for the multiple protein domains. Plant Cell 6:487–500
Mori M, Nomura T, Ooka H, Ishizaka M, Yokota T, Sugimoto K, Okabe K, Kajiwara H, Satoh K, Yamamoto K, Hirochika H, Kikuchi S (2002) Isolation and characterization of a rice dwarf mutant with a defect in brassinosteroid biosynthesis. Plant Physiol 130:1152–1161
Neer EJ, Schmidt CJ, Nambudripad R, Smith TF (1994) The ancient regulatory-protein family of WD-repeat proteins. Nature 371:297–300
Nonomura K, Nakano M, Fukuda T, Eiguchi M, Miyao A, Hirochika H, Kurata N (2004a) The novel gene HOMOLOGOUS PAIRING ABERRATION IN RICE MEIOSIS1 of rice encodes a putative coiled-coil protein required for homologous chromosome pairing in meiosis. Plant Cell 16:1008–1020
Nonomura KI, Nakano M, Murata K, Miyoshi K, Eiguchi M, Miyao A, Hirochika H, Kurata N (2004b) An insertional mutation in the rice PAIR2 gene, the ortholog of Arabidopsis ASY1, results in a defect in homologous chromosome pairing during meiosis. Mol Genet Genomics 271:121–129
Nonomura K, Nakano M, Eiguchi M, Suzuki T, Kurata N (2006) PAIR2 is essential for homologous chromosome synapsis in rice meiosis I. J Cell Sci 119:217–225
Reiner O, Carrozzo R, Shen Y, Wehnert M, Faustinella F, Dobyns WB, Caskey CT, Ledbetter DH (1993) Isolation of a Miller–Dieker lissencephaly gene containing G protein beta-subunit-like repeats. Nature 364:717–721
Reiner O, Sapoznik S, Sapir T (2006) Lissencephaly 1 linking to multiple diseases: mental retardation, neurodegeneration, schizophrenia, male sterility, and more. Neuromolecular Med 8:547–565
Sato Y, Sentoku N, Miura Y, Hirochika H, Kitano H, Matsuoka M (1999) Loss-of-function mutations in the rice homeobox gene OSH15 affect the architecture of internodes resulting in dwarf plants. EMBO J 18:992–1002
Shan JX, Zhu MZ, Shi M, Gao JP, Lin HX (2009) Fine mapping and candidate gene analysis of spd6 responsible for small panicle and dwarfness in wild rice (Oryza rufipogon Griff.). Theor Appl Genet 119:827–836
Shi DQ, Liu J, Xiang YH, Ye D, Sundaresan V, Yang WC (2005) SLOW WALKER1, essential for gametogenesis in Arabidopsis, encodes a WD40 protein involved in 18S ribosomal RNA biogenesis. Plant Cell 17:2340–2354
Smith TF, Gaitatzes C, Saxena K, Neer EJ (1999) The WD repeat: a common architecture for diverse functions. Trends Biochem Sci 24:181–185
Sondek J, Bohm A, Lambright DG, Hamm HE, Sigler PB (1996) Crystal structure of a G-protein beta gamma dimer at 2.1 Å resolution. Nature 379:369–374
Sorensen MB, Chaudhury AM, Robert H, Bancharel E, Berger F (2001) Polycomb group genes control pattern formation in plant seed. Curr Biol 11:277–281
Tai CY, Dujardin DL, Faulkner NE, Vallee RB (2002) Role of dynein, dynactin, and CLIP-170 interactions in LIS1 kinetochore function. J Cell Biol 156:959–968
Ullah H, Chen JG, Temple B, Boyes DC, Alonso JM, Davis KR, Ecker JR, Jones AM (2003) The beta-subunit of the Arabidopsis G protein negatively regulates auxin-induced cell division and affects multiple developmental processes. Plant Cell 15:393–409
van Nocker S, Ludwig P (2003) The WD-repeat protein superfamily in Arabidopsis: conservation and divergence in structure and function. BMC Genomics 4:50
von Arnim AG, Osterlund MT, Kwok SF, Deng XW (1997) Genetic and developmental control of nuclear accumulation of COP1, a repressor of photomorphogenesis in Arabidopsis. Plant Physiol 114:779–788
Wang H, Ma LG, Li JM, Zhao HY, Deng XW (2001) Direct interaction of Arabidopsis cryptochromes with COP1 in light control development. Science 294:154–158
Wang L, Xie W, Chen Y, Tang W, Yang J, Ye R, Liu L, Lin Y, Xu C, Xiao J, Zhang Q (2010a) A dynamic gene expression atlas covering the entire life cycle of rice. Plant J 61:752–766
Wang M, Wang K, Tang D, Wei C, Li M, Shen Y, Chi Z, Gu M, Cheng Z (2010b) The central element protein ZEP1 of the synaptonemal complex regulates the number of crossovers during meiosis in rice. Plant Cell 22:417–430
Wei X, Xu J, Guo H, Jiang L, Chen S, Yu C, Zhou Z, Hu P, Zhai H, Wan J (2010) DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiol 153:1747–1758
Wu C, Li X, Yuan W, Chen G, Kilian A, Li J, Xu C, Zhou DX, Wang S, Zhang Q (2003) Development of enhancer trap lines for functional analysis of the rice genome. Plant J 35:418–427
Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X, Zhang Q (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40:761–767
Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572
Yuan W, Li X, Chang Y, Wen R, Chen G, Zhang Q, Wu C (2009) Mutation of the rice gene PAIR3 results in lack of bivalent formation in meiosis. Plant J 59:303–315
Zhang D, Wilson ZA (2009) Stamen specification and anther development in rice. Chin Sci Bull 54:2342–2352
Zhang J, Li C, Wu C, Xiong L, Chen G, Zhang Q, Wang S (2006a) RMD: a rice mutant database for functional analysis of the rice genome. Nucleic Acids Res 34:D745–D748
Zhang L, Tao J, Wang S, Chong K, Wang T (2006b) The rice OsRad21–4, an orthologue of yeast Rec8 protein, is required for efficient meiosis. Plant Mol Biol 60:533–554
Zhang J, Guo D, Chang Y, You C, Li X, Dai X, Weng Q, Chen G, Liu H, Han B, Zhang Q, Wu C (2007) Non-random distribution of T-DNA insertions at various levels of the genome hierarchy as revealed by analyzing 13 804 T-DNA flanking sequences from an enhancer-trap mutant library. Plant J 49:947–959
Zhang DS, Liang WQ, Yuan Z, Li N, Shi J, Wang J, Liu YM, Yu WJ, Zhang DB (2008) Tapetum degeneration retardation is critical for aliphatic metabolism and gene regulation during rice pollen development. Mol Plant 1:599–610
Zhang H, Liang W, Yang X, Luo X, Jiang N, Ma H, Zhang D (2010) Carbon starved anther encodes a MYB domain protein that regulates sugar partitioning required for rice pollen development. Plant Cell 22:672–689
Zhou S, Wang Y, Li W, Zhao Z, Ren Y, Gu S, Lin Q, Wang D, Jiang L, Su N, Zhang X, Liu L, Cheng Z, Lei C, Wang J, Guo X, Wu F, Ikehashi H, Wang H, Wan J (2011) Pollen semi-sterility1 encodes a kinesin-1-like protein important for male meiosis, anther dehiscence, and fertility in rice. Plant Cell 23:111–129
Acknowledgments
We thank Dr. Jian Xu for providing the plasmid pM999 and Dr. Gynheung An for providing the T-DNA insertional line 3A-04974. We thank Dr. Meizhong Luo for providing the Zhonghua 11 genomic DNA BAC clone a0023F18. This research was supported by grants from Program for New Century Excellent Talents in University, the National Natural Science Foundation of China, and the Key Project on Plant Transgenic Research.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Gao, X., Chen, Z., Zhang, J. et al. OsLIS-L1 encoding a lissencephaly type-1-like protein with WD40 repeats is required for plant height and male gametophyte formation in rice. Planta 235, 713–727 (2012). https://doi.org/10.1007/s00425-011-1532-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-011-1532-7