Glabrous Rice 1, encoding a homeodomain protein, regulates trichome development in rice
- Jinjun Li†1,
- Yundong Yuan†2,
- Zefu Lu2,
- Liusha Yang2,
- Rongcun Gao1,
- Jingen Lu1,
- Jiayang Li2 and
- Guosheng Xiong2Email author
© li et al.; licensee Springer. 2012
Received: 30 March 2012
Accepted: 27 September 2012
Published: 6 October 2012
Glabrous rice, which lacks trichomes on the rice epidermis, is regarded as an important germplasm resource in rice breeding. Trichomes are derived from aerial epidermal cells and used as a model to study the cell fate determination in plant. In Arabidopsis, the molecular mechanisms of trichome development have been well studied. However, little is known about the molecular basis of trichome development in rice.
In this study, near isogenic lines harboring the glabrous rice 1 locus were developed. By a map-based approach, we narrowed down the locus to a 21-kb DNA region harboring two genes. One of the genes named Glabrous Rice 1 (GLR1), which is most likely the candidate, encodes a homeodomain protein containing the WOX motif. Constitutive Expression of GLR1 could partially complement the glabrous phenotype of NIL glr1 . The knock down of GLR1 by RNA interference led to a significant decrease in trichome number on the leaves and glumes of the RNAi transgenic plants.
GLR1 plays an important role in rice trichome development and will contribute to breeding of glabrous elite rice varieties.
KeywordsGlabrous rice Trichome development WOX protein
The glabrous feature of rice is considered as a favorite agronomic trait for rice farmers because it has greater packing capability of rice grains and produces less dust that causes itching effect on farmers. Glabrous rice lacks trichomes on leaves and glumes (Khush, et al.2001). Most rice cultivars in America are glabrous and recognized as an important germplasm resource in breeding due to its high yield, good quality, and wide compatibility in crossing with other rice varieties (Guoet al.1999, Luo et al.2000). Trichomes are derived from aerial epidermal cells and serve various protective purposes such as insect herbivore resistance, freezing tolerance, and shade of UV irradiation (Ishida et al. 2008). There are two distinct types of trichomes developed on leaves of monocot plants. One is macrohairs on silica cells, the other is microhairs along the stomata cells (Khush, et al. 2001). So far, a number of glabrous mutants have been identified in many plant species, including Arabidopsis, tomato, cotton, and maize (Machado et al.2009, Moose et al.2004, Rerie et al.1994, Yang et al.2011). However, the molecular mechanism underlying trichome development has only been intensively investigated in Arabidopsis.
In Arabidopsis, trichome development has been used as a model system to study the cell fate determination and shown to be regulated by a complex gene network (Ishida et al.2008). A homeodomain-leucine zipper protein GLABRA2 (GL2) and an R3 Myb protein TRIPTYCHON (TRY) play essential roles in trichome initiation and hairless cell differentiation (Rerie et al. 1994, Schellmann et al. 2002). The expression of GL2 and TRY are regulated by the WD-repeat/bHLH/MYB complex including TRANSPARENT TESTA GLABRA1 (TTG1), GLABRA3 (GL3)/ENHANCER OF GLABRA3 (EGL3) and GLABRA1 (GL1). Epidermal cells expressing the GL2 protein are able to differentiate into trichome cells. The TRY protein expressed in trichome cells, however, can move into neighboring cells and compete with GL1 for binding to GL3/EGL3 to repress the GL2 expression. The TRY mediated down regulation of the GL2 expression inhibits trichome formation in neighboring cells (Ishida, et al. 2008). Actually, factors able to modulate this gene network affect the trichome development. Previous studies on mutants defective in the biosynthesis and/or signaling of gibberellins, salicylic acid, jasmonic acid, and cytokinin have showed that phytohormones are involved in trichome initiation (Gan et al.2006, Gan et al.2007b, Perazza et al.1998, Traw and Bergelson 2003, Zhou et al.2011). It has been turned out that roles of these phytohormones in trichome development are mediated by their effect on the expression or activity of the components of the WD-repeat/bHLH/MYB complexes. Roles of gibberellins and cytokinins in trichome initiation are mainly dependent on C2H2 transcription factors including GIS1, GIS2, ZFP5 and ZFP8. These transcription factors are able to promote the GL1 expression (Gan et al.2007a, Maes et al.2008, Perazza, et al.1998, Zhou, et al.2011). In addition, JAZ proteins, the key components in the JA signaling pathway, have been shown to interact with bHLH transcription factors (GL3, EGL3 and TT8) and MYB transcription factors (MYB75 and GL1) (Qi et al.2011). The JA-induced destruction of JAZ proteins results in releasing the transcriptional function of the WD-repeat/bHLH/MYB complex and activating downstream events of trichome initiation. Furthermore, recent studies have shown that the microRNA156 targeted gene SPL9 could bypass the function of GL1 and directly binds to promoters of TCL1 and TRY to activate their expression (Yu et al.2010).
In contrast to the sophisticated mechanisms revealed in Arabidopsis, little is known about the molecular mechanisms of trichome development in other plants. It has been noted that a couple of homeodomain-leucine zipper proteins, which are specifically expressed in epidermal cells, are essential in differentiation of epidermal cells. Outer Cell Layer 4 (OCL4), a maize HD-ZIP transcription factor, has been suggested to involve in the repression of macrohair differentiation (Vernoud, et al. 2009), and a HD-Zip protein in tomato, Woolly (Wo) that interacts with Cyclin B2, plays an essential role for trichome formation and embryonic development (Yang et al. 2011). In addition, another subfamily of the homeobox gene, known as WUS-like homeobox genes (WOX), may also play roles in division or differentiation of epidermal cells. Pressed Flower (PRS) is involved in activation of the proliferation of marginal cells. It has been observed that multicellular bulges with trichomes formed on stems and epidermal cells outgrow on sepals of 35S:PRS transgenic plants (Matsumoto and Okada 2001). Moreover, Narrow sheath 1 (NS1) and Narrow sheath 2 (NS2), which are duplicated relatives of PRS in maize, have been suggested to play a role in a lateral domain of shoot apical meristems (Nardmann et al.2004). In addition, OsWOX3 has been found to repress the expression of OsYAB3, which is required for cell differentiation during rice leaf development (Dai et al.2007).
Previous study showed that macrohairs on the leaf blade are greatly reduced in the maize macrohairless 1 (mhl1) mutant (Moose, et al.2004). A major QTL controlling macrohairs in Teosinte has been found to locate near the maize gene MHL1 (Lauter et al.2004). In rice, previous genetic analysis has identified a couple of loci that control trichome development. For example, gl regulates glabrous leaf and hull traits, Hl a and Hl b were related to long hair development on rice leaves and Hg may be responsible for the extreme long hairs on auricles and glumes (Nagao et al.1960). However, no gene controlling these traits has been cloned in rice as yet. Recently, glabrous leaf and hull mutant (gl1) has been reported to locate within a 54-kb region at the short arm of chromosome 5 (Li et al.2010, Wang et al.2009, Yu et al.1995), but the gene has not been identified yet. Here, we report the identification and characterization of the Glabrous Rice 1 (GLR1), which controls the trichome development in rice. Our work extends an insight into the molecular mechanism of trichome development in rice. The identification and characterization of GLR1 will facilitate breeders to develop elite glabrous rice varieties via marker-assisted-selection and genetic modification approaches.
Phenotype of the near isogenic line of glabrous rice
Map-based cloning of GLR1
Molecular markers developed in this study
Altering the expression levels of GLR1 could partially change the glabrous phenotype
DNA methylation may be involved in the expression of GLR1
In Arabidopsis, trichomes have been served as an excellent model system to study plant cell differentiation (Ishida et al. 2008). Glabrous mutants that are defective in leaf hair or trichome have been identified in many plant species. However, genes controlling trichome development in rice have not been identified up to date yet. GL1 was previously mapped on the short arm of chromosome 5 (Li, et al. 2010, Wang et al. 2009, Yu et al. 1995) and it was proposed that a single nucleotide mutation (A to T) in the 5’UTR of LOC_Os05g02754 (Os05g0118900), which encode an unknown protein, might be responsible for the gl1 trait (Li, et al. 2010). Our mapping data suggested that glr1 may be allelic to gl1. We compared the sequences of 5’UTR of LOC_Os05g02754 (Os05g0118900) of NIL GLR1 and NIL glr1 and found that the indicated position of 5’ UTR of LOC_Os05g02754 (Os05g0118900) in the NIL GLR1 plant is A and that in the NIL glr1 plant is T. However, our data indicate that instead of LOC_Os05g02754 (Os05g0118900) LOC_Os05g02730 (Os05g0118700), which encode a WUS-like homeodomain protein, controls the glabrous phenotype. First, the mapping data has pinpointed the GLR1 locus within a 21-kb region that contains only two predicted genes, LOC_Os05g02720 (Os05g0118600) and LOC_Os05g02730 (Os05g0118700). Second, comparison of the gene expression levels of LOC_Os05g02720 and LOC_Os05g02730 between NIL GLR1 and NIL glr1 plants showed that LOC_Os05g02730 is dramatically increased in the NIL glr1 plant, however, change of LOC_Os05g02720 in the NIL glr1 plant is not very significant. In contrast, no difference of expression levels of LOC_Os05g02754 has been detected between NIL GLR1 and NIL glr1 plants (Figure 2d). Third, an apparent decrease in the trichome number on leaves and glumes of GLR1 RNAi transgenic plants have been obtained. Overexpression of GLR1 in NIL glr partially rescues glabrous phenotype of the NIL glr1 plant. Fourth, the sequence alignment showed that GLR1 has high similarity to previously identified homeodomain proteins, whose functions are essential for the differentiation of epidermal cells (Dai, et al. 2007, Matsumoto and Okada 2001, Nardmann, et al. 2004). Taken all these together, we strongly suggest that the WUS-like homeodomain protein encoded by LOC_Os05g02730 is the GLR1 gene and is essential for the trichome development in rice.
The RNAi of GLR1 reduced the trichome number in transgenic lines, while the trichome is almost completely lost in NIL glr1 . This discrepancy could result from the different genetic background of plant materials or from incomplete suppression of the target gene in transgenic plants. Alternatively, the expression LOC_Os05g02720 is also decreased in the NIL glr1 plant, which implies that LOC_Os05g02720 may be also involve in trichome development, thus knockdown of LOC_Os05g02730 alone cannot completely suppress the trichome development. Further knockdown LOC_Os05g02720 along or knockdown it together with LOC_Os05g02730 will clarify the role of LOC_Os05g02720.
Chromatin state controls gene expression and plays critical roles in development. In plant, trimethylated K9 of histone H3 (H3K9me3) indicates an open chromatin state, while monomethylated and dimethylated H3K9s (H3K9me1 and H3K9me2) indicate a closed state (Liu et al. 2010). The identification of GL2 EXPRESSION MODULATOR (GEM) indicates that the regulation of GL2 expression is more complicated than previously expected (Caro, et al. 2007). Trichome density increased in gem-1 mutant whereas decreased in GEM-overexpressing plants. Consistent with the phenotype, the GL2 expression has been observed to increase in gem-1 whereas decrease in GEM-overexpressing plants (Caro, et al. 2007). It has been observed that H3K9me3 increases and H3K9me2 decreases in the GL2 promoter in the gem-1 background, but H3K9me3 decreases and H3K9me2 increases in GEM-overexpressing plants (Caro, et al. 2007). This kind of epigenetic control may also be involved in rice trichome development. Rice SET Domain Group Protein 714 (SDG714) functions as a histone H3K9 methyltransferase, which is involved in histone H3K9 methylation, DNA methylation and genome stability (Ding et al. 2007). Loss of macrohairs but not microhairs on leaves of the SDG714 RNAi transgenic plants indicated that regulation of chromatin status of some unidentified regulators may play an important role in the trichome development in rice (Ding et al.2007). In agreeable to these findings, the genomic bisulfite sequencing of GLR1 showed that the DNA methylation pattern at several sites of the GLR1 promoter region in the NIL glr1 plants is different from that in the NIL GLR 1 plants, though no sequence difference of GLR1 was found between the NIL GLR 1 and NIL glr1 plants. These results indicated that the epigenetic mechanism may be involved in the regulation of the GLR1 expression and the trichome development in rice. Although, different patterns of the DNA methylation in upstream region of LOC_Os05g02730 (Os05g0118700) between NIL GLR1 and NIL glr1 has been observed, we are unable to determine which sites are responsible for suppression of LOC_Os05g02730. Moreover, the GLR1 expression driven by a constitutive promoter dramatically increased the expression of GLR1, but cannot completely rescue the glabrous phenotype in T0 transgenic plants (Figure 4 d-g). It indicates that the regulation of the GLR1 expression and the trichome development in rice is more complicate than expected. Further investigation is needed to uncover the molecular mechanism of GLR1 expression regulation.
Glabrous rice varieties are widely cultivated in America and Africa, while most varieties cultivated in Asia are pubescent (Khush, et al.2001). In higher plants, although trichomes are thought to be important for plant defense against biotic and abiotic stresses, glabrous trait may be a selectively neutral trait in rice. Previous studies have indicated that the introduction of glabrous trait into japonica varieties may not cause any obvious disadvantages in plant defense (Li et al.2011). In agriculture, the interest of breeding glabrous elite rice varieties is mainly due to its practical advantages of greater packing capability and less itching effect during the harvest process. The cloning of GLR1 will not only help to understand the molecular mechanism of trichome development in rice but also improve the efficiency of breeding glabrous elite rice varieties by marker-assisted selection and genetic modification approaches.
GLR1 plays an important role in rice trichome development and will contribute to breeding of glabrous elite rice varieties
Jia64 is a glabrous variety derived from American rice variety Rico No.1 and Jia33 is a pubescent variety in southeast China. Rice plants were cultivated in the experimental field of Jiaxing Academy of Agricultural Science in growing seasons from May to October.
Scanning electron microscopy
Samples were prepared as described previously (Li et al.2009). Briefly, samples were fixed with 2.5% (v/v) glutaraldehyde in 0.1 M sodium phosphate buffer (PBS, pH 7.2) at 4°C overnight. After being rinsed with 0.1 M PBS twice, samples were post-fixed in 1% (w/v) osmium tetroxide for 2 h at 4°C. Samples were rinsed with the same buffer for 2 more times and then dehydrated in a graded series of ethanol. For scanning electron microscopy, samples were critical-point dried (Hitachi HCP-2) and observed under a scanning electron microscope (Hitachi S-3000N).
Genetic mapping of GLR1
An F2 mapping population was generated from a cross between Jia64 and Jia33. 24 molecular markers were used for genetic linkage analysis of 44 F2 plants that show the glabrous phenotype. To fine-map GLR1, new PCR-based markers were developed and 1,447 F2 glabrous plants were analyzed using markers as given in Table 1. The GLR1 locus was further narrowed within an interval of 21-kb DNA fragment between the M6 and M7 markers. To sequence the GLR1 locus, the entire genomic region was amplified from NIL GLR1 and NIL glr1 by PCR with LA-Taq (TaKaRa).
RNA extraction and reverse transcription-polymerase chain reaction (RT-PCR)
Primers for RT-PCR and RNAi construct
Primer sequence (5′-3′)
Plasmid construction and rice transformation
To generate the RNAi construct, two DNA fragments RNAi 1-1 and RNAi 1-2 were amplified respectively by primers RNAi 1-1f and RNAi1-1r, RNAi1-2f and RNAi1-2r (Table 2). The construct 1460-RNAi 1-1 was generated by digesting the RNAi 1-1 fragment with Bam H I and Kpn I and ligated to the binary vector 1460 by T4 DNA ligases. The hairpin cassette was generated by digesting the RNAi 1-2 fragment with Sac I and Spe I and ligated in reversed direction of fragment RNAi 1-1 to construct 1460-RNAi 1-1. For construction of the overexpression cassette, the coding region of GLR1 was amplified and liagated to the 1460 vector by BamH I and Spe I. The constructs were confirmed by sequencing and introduced into Agrobacterium tumefaciens strain EHA105 by electroporation. The rice (Nipponbare) transformation was performed as described previously (Hiei et al.1994). For RNAi transgenic plants, T2 lines derived from individual transgenic lines were used for further analysis. T2 Lines RNAi 4-8-7, RNAi 4-8-11 and RNAi 4-8-17 were derived from line RNAi 4-8. T2 Lines RNAi 4-9-4 and RNAi 4-9-11 were derived from line RNAi 4-9. For overexpression transgenic plants, T0 plants were used for analysis.
Primers for Bisulfite sequencing
This work is supported by grants (2010C12002 and 011102471) from Department of Science and Technology of Zhejiang Province.
- Caro E, Castellano MM, Gutierrez C: A chromatin link that couples cell division to root epidermis patterning in Arabidopsis . Nature 2007, 447: 213–217. 10.1038/nature05763View ArticlePubMedGoogle Scholar
- Dai M, Hu Y, Zhao Y, Liu H, Zhou DX: A WUSCHEL-LIKE HOMEOBOX gene represses a YABBY gene expression required for rice leaf development. Plant Physiol 2007, 144: 380–390. 10.1104/pp.107.095737PubMed CentralView ArticlePubMedGoogle Scholar
- Ding Y, Wang X, Su L, Zhai J, Cao S, Zhang D, Liu C, Bi Y, Qian Q, Cheng Z, Chu C, Cao X: SDG714, a histone H3K9 methyltransferase, is involved in Tos17 DNA methylation and transposition in rice. Plant Cell 2007, 19: 9–22. 10.1105/tpc.106.048124PubMed CentralView ArticlePubMedGoogle Scholar
- Gan Y, Kumimoto R, Liu C, Ratcliffe O, Yu H, Broun P: GLABROUS INFLORESCENCE STEMS modulates the regulation by gibberellins of epidermal differentiation and shoot maturation in Arabidopsis . Plant Cell 2006, 18: 1383–1395. 10.1105/tpc.106.041533PubMed CentralView ArticlePubMedGoogle Scholar
- Gan Y, Liu C, Yu H, Broun P: Integration of cytokinin and gibberellin signalling by Arabidopsis transcription factors GIS, ZFP8 and GIS2 in the regulation of epidermal cell fate. Development 2007, 134: 2073–2081. 10.1242/dev.005017View ArticlePubMedGoogle Scholar
- Gan Y, Yu H, Peng J, Broun P: Genetic and molecular regulation by DELLA proteins of trichome development in Arabidopsis . Plant Physiol 2007, 145: 1031–1042. 10.1104/pp.107.104794PubMed CentralView ArticlePubMedGoogle Scholar
- Guo L, Luo L, Zhong D, Yu X, Mei H, Wang Y, Ying C: Evaluation, improvement and utilization on some selected American rice cultivars. J Zhejiang Agric Sci 1999, 5: 201–206.Google Scholar
- Hiei Y, Ohta S, Komari T, Kumashiro T: Efficient transformation of rice ( Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 1994, 6: 271–282. 10.1046/j.1365-313X.1994.6020271.xView ArticlePubMedGoogle Scholar
- Ishida T, Kurata T, Okada K, Wada T: A genetic regulatory network in the development of trichomes and root hairs. Annu Rev Plant Biol 2008, 59: 365–386. 10.1146/annurev.arplant.59.032607.092949View ArticlePubMedGoogle Scholar
- Khush GS, Brar DS, Hardy B: Rice genetics IV. Proceedings of the Fourth International Rice Genetics Symposium, 22–27 October 2000, Los Baños, Philippines. Science Publishers, Inc, Enfield, NH (USA); 2001:29. Los Baños (Philippines): International Rice Research Institute Los Baños (Philippines): International Rice Research InstituteGoogle Scholar
- Lauter N, Gustus C, Westerbergh A, Doebley J: The inheritance and evolution of leaf pigmentation and pubescence in teosinte . Genetics 2004, 167: 1949–1959. 10.1534/genetics.104.026997PubMed CentralView ArticlePubMedGoogle Scholar
- Li J, Lin Z, Chen H, Xu M: The inheritance of glabrous-leaf character in rice variety Rico No. 1. Acta Agriculturae Zhejiangensis 1993, 5: 233–234.Google Scholar
- Li JJ, Tao R, Shi J, Hao Z, Gao R, Li L: Resistance identification of the rice varieties in southeastern China to rice stripe disease. Acta Phytophylacica Sinica 2011, 38: 221–226.Google Scholar
- Li S, Qian Q, Fu Z, Zeng D, Meng X, Kyozuka J, Maekawa M, Zhu X, Zhang J, Li J, Wang Y: Short panicle1 encodes a putative PTR family transporter and determines rice panicle size. Plant J 2009, 58: 592–605. 10.1111/j.1365-313X.2009.03799.xView ArticlePubMedGoogle Scholar
- Li W, Wu J, Weng S, Zhang D, Zhang Y, Shi C: Characterization and fine mapping of the glabrous leaf and hull mutants ( gl1 ) in rice ( Oryza sativa L.). Plant Cell Rep 2010, 29: 617–627. 10.1007/s00299-010-0848-2View ArticlePubMedGoogle Scholar
- Liu C, Lu F, Cui X, Cao X: Histone methylation in higher plants. Annu Rev Plant Biol 2010, 61: 395–420. 10.1146/annurev.arplant.043008.091939View ArticlePubMedGoogle Scholar
- Luo J, Hu P, Tang S, Fasong H: American glabrous rice utilized in breeding of super-high-yielding and good-quality varieties. Chin Rice Res Newsl 2000, 8: 3–5.Google Scholar
- Machado A, Wu Y, Yang Y, Llewellyn DJ, Dennis ES: The MYB transcription factor GhMYB25 regulates early fibre and trichome development. Plant J 2009, 59: 52–62. 10.1111/j.1365-313X.2009.03847.xView ArticlePubMedGoogle Scholar
- Maes L, Inze D, Goossens A: Functional specialization of the TRANSPARENT TESTA GLABRA1 network allows differential hormonal control of laminal and marginal trichome initiation in Arabidopsis rosette leaves. Plant Physiol 2008, 148: 1453–1464. 10.1104/pp.108.125385PubMed CentralView ArticlePubMedGoogle Scholar
- Matsumoto N, Okada K: A homeobox gene, PRESSED FLOWER , regulates lateral axis-dependent development of Arabidopsis flowers. Genes Dev 2001, 15: 3355–3364. 10.1101/gad.931001PubMed CentralView ArticlePubMedGoogle Scholar
- Moose SP, Lauter N, Carlson SR: The maize macrohairless1 locus specifically promotes leaf blade macrohair initiation and responds to factors regulating leaf identity. Genetics 2004, 166: 1451–1461. 10.1534/genetics.166.3.1451PubMed CentralView ArticlePubMedGoogle Scholar
- Nagao S, Takahashi M-E, Kinoshita T: Genetical studies on rice plant, XXV: inheritance of threemorphological characters, pubescence of leaves and floral glumes, and deformation of empty glumes. Journal of the Faculty of Agriculture, Hokkaido University; 1960:299–314.Google Scholar
- Nardmann J, Ji J, Werr W, Scanlon MJ: The maize duplicate genes narrow sheath1 and narrow sheath2 encode a conserved homeobox gene function in a lateral domain of shoot apical meristems. Development 2004, 131: 2827–2839. 10.1242/dev.01164View ArticlePubMedGoogle Scholar
- Perazza D, Vachon G, Herzog M: Gibberellins promote trichome formation by up-regulating GLABROUS1 in Arabidopsis . Plant Physiol 1998, 117: 375–383. 10.1104/pp.117.2.375PubMed CentralView ArticlePubMedGoogle Scholar
- Qi T, Song S, Ren Q, Wu D, Huang H, Chen Y, Fan M, Peng W, Ren C, Xie D: The Jasmonate-ZIM-domain proteins interact with the WD-Repeat/bHLH/MYB complexes to regulate Jasmonate-mediated anthocyanin accumulation and trichome initiation in Arabidopsis thaliana . Plant Cell 2011, 23: 1795–1814. 10.1105/tpc.111.083261PubMed CentralView ArticlePubMedGoogle Scholar
- Rerie WG, Feldmann KA, Marks MD: The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes Dev 1994, 8: 1388–1399. 10.1101/gad.8.12.1388View ArticlePubMedGoogle Scholar
- Schellmann S, Kirik SA, V Wada T, Okada K, Beermann A, Thumfahrt J, Jurgens G, Hulskamp M: TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J 2002, 21: 5036–5046. 10.1093/emboj/cdf524PubMed CentralView ArticlePubMedGoogle Scholar
- Traw MB, Bergelson J: Interactive effects of jasmonic acid, salicylic acid, and gibberellin on induction of trichomes in Arabidopsis. Plant Physiol 2003, 133: 1367–1375. 10.1104/pp.103.027086PubMed CentralView ArticlePubMedGoogle Scholar
- Vernoud V, Laigle G, Rozier F, Meeley RB, Perez P, Rogowsky PM: The HD-ZIP IV transcription factor OCL4 is necessary for trichome patterning and anther development in maize. Plant J 2009, 59: 883–894. 10.1111/j.1365-313X.2009.03916.xView ArticlePubMedGoogle Scholar
- Wang D, Sun S-X, Gao F-Y, Lu X-J, Li Z-H, Ren G-J: Mapping a rice Glabrous gene using simple sequence repeat markers. Rice Sci 2009, 16: 93–98. 10.1016/S1672-6308(08)60063-3View ArticleGoogle Scholar
- Yang C, Li H, Zhang J, Luo Z, Gong P, Zhang C, Li J, Wang T, Zhang Y, Lu Y, Ye Z: A regulatory gene induces trichome formation and embryo lethality in tomato. Proc Natl Acad Sci USA 2011, 108: 11836–11841. 10.1073/pnas.1100532108PubMed CentralView ArticlePubMedGoogle Scholar
- Yu N, Cai WJ, Wang S, Shan CM, Wang LJ, Chen XY: Temporal control of trichome distribution by microRNA156-targeted SPL genes in Arabidopsis thaliana . Plant Cell 2010, 22: 2322–2335. 10.1105/tpc.109.072579PubMed CentralView ArticlePubMedGoogle Scholar
- Yu ZH, McCouch SR, Tanksley SD, Kinoshita T, Sato S: Association of morphological and RFLP markers in rice ( Oryza sativa L.). Genome 1995, 38: 566–574. 10.1139/g95-073View ArticlePubMedGoogle Scholar
- Zhou Z, An L, Sun L, Zhu S, Xi W, Broun P, Yu H, Gan Y: Zinc finger protein 5 is required for the control of trichome initiation by acting upstream of zinc finger protein 8 in Arabidopsis . Plant Physiol 2011, 157: 673–682. 10.1104/pp.111.180281PubMed CentralView ArticlePubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.