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MYB26 Gene in Male Sterile and Another Dehiscence - Literature review Example

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The review "MYB26 Gene in Male Sterile and Another Dehiscence" focuses on the critical analysis of the major role of the MYB26 gene in developing male sterile and another dehiscence. Arabidopsis thaliana is a small flowering plant belonging to the family Brassicaceae…
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MYB26 Gene in Male Sterile and Another Dehiscence
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?Literature review: Analysis MYB26 gene and male sterility and anther dehiscence in A. thaliana Arabidopsis thaliana plant Arabidopsis thaliana, commonly known as Thale cress and Mouse-ear cress, is a small flowering plant (figure 1) belonging to family Brassicaceae (mustard or crucifer family). It is an annual weed (rarely biannual) originated in Europe, Asia and north western Africa and in temperate regions of the world (NASC, 2011). It is naturally found in poor sandy or gravelly soil and can find in wastelands, car parks and railway sides. Plant height at maturity is around 20-25cm and it produces small white flowers 3mm in diameter and is naturally self-pollinated. The Arabidopsis plant produce flowers from April to early June. The plants of this family are known as crucifers due to their uniform flower structure that resembles a ‘cross’ and are also characterized by a fruit named silique which is 5-20mm long with 20-30 seeds. The leaves are alternate (rarely opposite) and sometimes organized in basal rosettes. Figure 1. Arabidopsis thaliana plant: Left, the vegetative stage, before flowering and growth of the floral stalk (bottom left). On the centre an adult plant at full flowering/seed set. On the right, flower, floral stem and seeds. White bars represent 1 cm, except for flower and seeds: 1 mm. (image from http://www-ijpb.versailles.inra.fr/en/arabido/arabido.htm) Taxonomy of A. thaliana Genus Arabidopsis has several species but A. thaliana (L.) Heynh. 2n=10 is the most studied as the model plant. Kingdom: Plantae Order: Brassicales Family: Brassicaceae Genus: Arabidopsis Species: Arabidopsis thaliana (L.) Heynh. Importance of A. thaliana as a model plant Though it has no significant economic value, A. thaliana is widely used as a model plant in studying a wide range of subjects in plant science. This was first proposed as a model plant by Friedrich Laibact in 1943 (Meyerowitz, 2001) and now it is used extensively in studies based on evolution, genetics, population genetics and plant development. It is widely applied in genetic transformation studies, chromosomal analysis, genetic mapping and genome sequencing work. One important trait that makes A. thaliana an ideal model plant in plant science research is its small genome size. It has only five chromosomes with 157 million base pairs (Bennet et al., 2003) and the genetic and physical maps of all five genes are available. This is useful for genetic sequencing and mapping. In fact the first plant genomes sequenced were of A. thaliana in the year 2000 where 115.4 mega bases of the 125mb genome were sequenced (“Analysis of the genome sequence of the flowering plant Arabidopsis thaliana”, 2000). Such information provides the basis of understanding molecular biology of many plant traits and research has defined the functions of its 27,000 genes and the 35,000 proteins they encode (Integr8, 2011). In addition, A. thaliana has a short life cycle (six weeks from seed germination to seed maturation), has prolific seed production and the plant can be easily cultivated in restricted space. A. thaliana can be efficiently transformed with Agrobacterium and large number of mutants is available (www.arabidopsis.org). This plant has thus become valuable in genome projects and facilitates molecular level understanding of the biology of a flowering plant. Since Arabidopsis thaliana is similar to many other plants, it is believed that the properties found in Arabidopsis likely to be found in other flowering plants too. Therefore analyzing the structure and functions about Arabidopsis genes will pave the pathway to study about other plant species. Arabidopsis Information Resources (TAIR), located in Carnegie Institute for Science Department of Plant Biology, USA maintain a genetic and molecular biology database of A. thaliana (www.arabidopsis.org). TAIR includes data on complete genome sequence with gene structure, gene product information, metabolism and gene expression, genome maps, genetic and physical markers, DNA and seed stocks and all information about Arabidopsis research community. Development of anthers and mechanism of anther dehiscence Anther development: stamen structure and pollen development The male reproductive organ of a flowering plant is the stamen which consists of an anther and a filament. Pollen development takes place in the anther while the filament transmits water and nutrients to the anther. Also the filament holds the anther in a suitable position which aid in pollen dispersal during dehiscence (Scott et al., 2004). Anther development begins when the stamen primodia in the third whorl of the floral meristem emerge (Goldberg et al., 1993). The third whorl of the Arabidopsis flower contains six stamens. Cells in the stamen primodia undergo specification and differentiate to produce mature anther cell types which generate anther and filament. Generally, anthers have a four-lobed structure with cell type pattern that is repeated in each lobe. Anthers of A. thaliana have a bilateral symmetry with four lobes, each with four distinct somatic cell layers (epidermis, endothecium, middle layer and tapetum). Tapetum comprises the inner surface of anther wall and provides nutrients, enzymes and materials needed for pollen development. It is also vital for the formation of pollen wall and pollen coat (Yang et al., 2007). Pollens are developed inside the anther where the male sporogenous cells differentiate into pollen mother cells (PMC, male meiocytes or microsporocytes) and undergo meiosis. During meiosis, these cells form tetrads of haploid microspores and the second phase of anther development occur which give rise to microspores. Microspores are generated in each lobe when the sporogenesis cells start meiosis and produce haploid microspores. When these microspores are released into anther locule, the development of male gametophyte begins (figure 2). Other cell types in the anther are involved in maturation and protection of pollen and anther dehiscence. When anthers are mature enough to produce the tricellular pollen grains, the filaments begin rapid elongation, anther enlarges and expands, cell degeneration initiates and the anther enter into the dehiscence program. Next step is the flower opening and release of mature pollen by anther dehiscence. Dehiscence results in the opening of the stomium region of anther wall and pollen grains are released. Pollen wall formation happens as two distinct layers; the ‘exine’ (outer part of the wall) and the internal intine (made from cellulose, protein and pectin) (Scott et al., 2004). The outer wall of spores, i.e. the exine and pollen grains get their strength from sporopollenin (a highly resistant polymer) which is synthesized in the tapetum (Quilichini et al., 2010). Figure 2. Anther Development. (Image from http://www.plantcell.org/cgi/content-nw/full/16/suppl_1/S46/FIG1) (A) Scheme of a transverse section through an Arabidopsis floral bud showing the number, position, and orientation of the floral organs (after Hill and Lord, 1989). (B) Schemes of transverse sections through Arabidopsis anthers at different stages (after Sanders et al., 1999). Floral stages are as described by Smyth et al. (1990); anther stages are as described by Sanders et al. (1999). C, connective; E, epidermis; En, endothecium; ML, middle layer; S, septum; St, stomium; StR, stomium region; T, tapetum; Td, tetrads; TPG, tricellular pollen grains; V, vascular bundle. Anther dehiscence Dehiscence of anthers is a multi-step procedure. It is the final action of anther that results in the release of pollen grains for pollination, fertilization and subsequent seed formation (Goldberg et al., 1993). This process precisely coordinates with the differentiation of pollen, floral development and flower opening (Sanders et al., 2000). Anther dehiscence begins with the degeneration of middle layer and tapetum (Scott et al., 2004) Next, the endothelical layers are expanded and fibrous bands (secondary wall thickenings) are deposited in endothelical and connective cells. During dehiscence, anther wall breaks at a specific site that run along the anther length, between two adjacent locules, the septum. The septum degenerates forming the bilocular anther followed by stomium cell breakage. Stomium is the opening of these locules by one slit and both stomium and septum are two special cell types involved in the dehiscence process. During the early stages of anther development, program of events initiates, resulting the breaking of stomium. First, the stomium and septum cells are differentiated from precursor cells between anther locules and then these cells undergo a timed cell degeneration program (Sanders et al., 1999). The septum separating the locules degenerates by enzymatic lyses, leaving stomium as the site for anther wall breakage to release pollen. Next, the stomium subsequently splits due to stresses associated with pollen swelling and dehydration of anthers to release pollen (Wilson et al. (2011). During microspore maturation, secondary cell wall thickening happens in the endothecium where cellulose, hemicelluloses and lignin are deposited in the epithelial cells. This secondary cell wall thickening is a vital requirement in many aspects in plant development like water transport, support and where mechanical forces are needed. It is essential for anther dehiscence since thickening of cell walls is important for endothecial cells to generate the physical force required for dehiscence (Dawson et al., 1999). Just before dehiscence, the epidermal and endothelical cells become turgid which generate the inwardly directed force in the anther wall, causing the weakened stomium to rupture. The desiccation of the endothecium then causes differential shrinkage of thickened and non-thickened parts of the cell wall, resulting in an outwardly bending force. This force leads to retract anther wall and the stomium is fully opened thereby permitting pollen release. Genes involved in anther development and dehiscence in A. thaliana MYB protein family is a large group of proteins present in all eukaryotes which functions mostly as transcription factors. MYB proteins are classified as R1, R2, R3 etc and in plants, members of R2R3 MYB family affect many plant-specific processes. In A. thaliana, the R2R3 MYB proteins are involved in controlling primary and secondary metabolism (AtMYB11/PFG1, AtMYB12/PFG2 and AtMYB111/PFG3 in flavonoid biosynthesis), in regulating plant developmental processes (AtMYB37/RAX1, AtMYB38/RAX2/BIT1 and AtMYB84/RAX3/ subgroup 14 in axillary meristem formation and AtMYB21, AtMYB24, AtMYB57 in anther development) and in regulating cell fate and identity (At MYB0 and AtMYB23 in controlling trichome initiation in shoots and AtMYB66 in controlling root hair patterning) (Dubos et al., 2010). AtMYB32 and AtMYB4 genes are members of R2R3-type MYB gene family and are involved in normal pollen development of A. thaliana (Preston et al., 2004). Expression of AtMYB32 is observed in many tissues, especially in anther tapetum, stigma papillae and lateral root primodia. When T-DNA inserted populations were analyzed, two mutants with partial male sterility were identified. The pollen grains were deformed and lacked cytoplasm. This deformation of popllen was observed in both AtMYB32 and AtMYB4 mutants. These workers concluded that change in the levels of AtMYB32 and AtMYB4 expression can influence pollen development through affecting pollen wall composition. AtMYB103 gene regulates tapetum and trichome development in A. thaliana (Li, et al., 2007). A FLOWER FLAVONOID TRANSPORTER (FFT) in A. thaliana (AtDTX35) is highly transcribed in floral tissues (anthers, stigma, nectarines, siliques)and a mutant analysis has shown that the correct development of the reproductive system of A. thaliana is disturbed in the absence of this transcriptor and hence affects pollen development and anther dehiscence (Thompson et al., 2010). The MALE STERILITY 1 (MS 1) gene is vital for tapetal development and microspore maturation. In ms1 mutant, the early stages of pollen mother cells (PMC) are normal but subsequently, microspores and tapetum get degenerated. The MALE STERILITY 2 (MS 2) gene is important for pollen wall formation. Kim, Jung and Park (2010) reported that Arabidopsis gene RMF (reduced male fertility) regulate tapedum and middle layer degeneration during anther development. RMF expression is notable in anthers and especially in pollen grains. Over-expression of RMF gene alters the plant phenotype and disturbs pollen maturity. Jung et al., (2007) postulates that the Arabidopsis histidine – controlling phosphor transfer proteins (AHP4s) are mediators in a multistep phosphorelay pathway for cytokinin hormone signaling and they negatively regulates thickening of the secondary cell wall of the anther endothecium. Over-expression of AHP4 gene reduced fertility due to lack of secondary wall thickening of the endothecium of Arabidopsis plants and inhibited the expression of IRXs, the xylem genes. Homeodomain proteins are an important group of transcription factors in plants. They are characterized by a 180-bp DNA sequence called homeobox (Gehring et al., 1994). Plant homeobox genes are a large family of transcription factors that play an important role in growth and development process. A. thaliana genome encodes 89 homeodomain proteins out of which 47 are HD-ZIP subfamily (Li et al, 2007). HDG3 is a member of class IV HD-ZIP subfamily genes. Mainly expressed in anthers, HDG3 plays a role in anther dehiscence. According to Li et al. (2007), HDG3 negatively regulate anther dehiscence by controlling the expression of MYB26, NST1 and NST2 directly or indirectly. As these are the three genes involved in anther dehiscence of Arabidopsis, (Steiner-Lange et al., 2003; Mitsuda et al., 2005 and Zhong and Ye, 2007), it is possible that HDG3 plays a role in non-dehiscence of anthers in A. thaliana. MYB26/MALE STERILE 35 (MS35) gene and its association with anther dehiscence A. thaliana MS35 gene, renamed as MYB26 gene (figure 3), is essential for the development of secondary thickening in anther endothecium and subsequent dehiscence (Yang et al., 2007). Located in the cell nucleus, this gene regulates endothelial development and secondary thickening in cell specific manner in anthers. MYB26 expression is observed in anthers, style and nectaries especially during early endothecial development, during pollen mitosis1 and during bicellular stages. Therefore its effect is more prominent in early endothelial development. A number of genes involved in secondary thickening are regulated by MYB26 gene i.e. XYLEM1 (IRX 1), IRX 3, IRX 8 and two NAC domain genes, NAC SECONDARY WALL PROMOTING FACTOR 1 (NST 1) and NST 2 (Yang et al., 2007) that are regulators of secondary wall thickening in anther walls and endothecium. Mitsuda et al. (2005) showed that expression of chimeric repressors from NAC transcription factors (NST1 and NST2) resulted in a defect in anther dehiscence due to failure in secondary wall thickening in anther endothecium. As the activity of NST2 promoter was specifically strong in anther tissues and NST1 promoter was present in many tissues with lignified secondary walls, they suggested that the NAC transcription factors as the possible regulators of secondary wall thickening in tissues. Therefore, MYB26 plays a regulatory role in endothecial cell development within anther and also in lignin biosynthesis pathway. Male sterility in A. thaliana Male sterility is the failure of plant to produce functional anthers, pollen or male gamates or it can be a failure in releasing viable pollen (Wilson et al., 2011). Usually, male sterility arise as cytoplasmic male sterility (CMS), nuclear (genetic) male sterility and genetic-cytoplasmic male sterility (Jain, 1959). CMS is maternally inherited while genetic-cytoplasmic male sterility involves genes from nucleus as well as from cytoplasm. The nuclear male sterility follows Mendelian inheritance pattern and thus important in crop breeding programs. In crop breeding programs where only hybrid seeds are desired, male sterility becomes really important as it prevent the need of manual emasculation which is a time and labour intensive process that is practiced to avoid self-fertilization. Male sterility occurs naturally or it can be induced by mutations in nuclear or cytoplasmic genes. Therefore, when natural male sterility is unavailable, inducing male sterility by genetic engineering becomes the other option. A detailed study by Sanders et al.(1999) revealed that A. thaliana male sterile mutants arises due to reasons such as defects in anther morphology, microspore production, defects in differentiation of anther cell types, pollen functions and anther dehiscence. They characterized 16 recessive male-sterile mutants belonging to different phenotypic classes. ‘Pollenless mutants’ were the result of defects in early anther developmental process and ‘dehiscence mutants’ were associated with the development and functioning of stomium region. Dehiscence mutants arise either due to ‘non-dehiscence’ where due to an abnormal cell death program during anther development, anther is unable to release (dehisce) the viable pollen or due to ‘delayed dehiscence’ where pollen is released later when stigmatic papillae are no longer receptive for pollination. It is important to note that in both cases, viable pollen are produced but the lack of ability to release them in appropriate manner give rise to male sterility. Several male sterile mutants in Arabidopsis have been listed in Sakata and Higashitani (2008). Among them, dad1 (defective in anther dehiscence 1), exs (extra sporogenous cells), ems 1(excess microsporocyto 1), tpd 1(tapedum determinant 1), mmd 1(male meiocyto death 1), serk 1&2 (somatic embryogenesis receptor kinase 1), ms1, dyt 1(dysfunctional tapedum),gne1, gne2 and myb26/ms35 are responsible for male sterile phenotypes whereas At Rad51 and At Spo11 has male and female sterility phenotypes. High temperature stress also causes male sterility in Arabidopsis by degradation of anther wall and arresting proliferation (Sakata and Higashitani, 2008). Two ‘pollenless’ mutants, pollenless3-1 (mutant with a T-DNA insert) and pollenless3-2 (mutant with a 1-kb deletion in the POLLENLESS gene) failed to produce viable microspores due to a defect in meiosis. Male sterility has occurred in A. thaliana due to pollen abortion after meiosis. As explained by Gaillard et al. (1998), the reason was a mutation in the APT1 gene resulting in adenine phosphoribosyl transferase activity (ARPT). Failure to elongate stamens just prior to anther dehiscence was postulated by Dawson et al. (1993) as the possible cause for male sterility in five Arabidopsis mutants induced by X-ray and Ethyl methane sulfonate (EMS) chemical mutagenesis. Bcp1 gene is a male specific gene responsible for pollen development and is active in tapetum and microspores. In a study aimed at restoring male sterility of A. thaliana, Tehseen et al. (2010) silenced Bcp1 using RNA interference technology (RNAi) revealing the possibility of artificially generating male sterility in plant breeding progrmmes as required. Jasmonic acid (JA) is a lipid – derived signaling compound that is widely distributed in the plant kingdom. It provides a critical signal for dehiscence and several mutants in JA biosynthetic enzymes cause male sterility which can be rescued by application of JA (Sanders et al., 2000; Park et al., 2002; van Malek et al., 2002). The DEFECTIVE IN ANTHER DEHISCENCE (DAD1) gene encodes a phospholipase A1 that catalyze the initial step of JA biosysthesis. Desiccation is delayed in anthers of dad1 mutant and hence, the locules of endothecium and connective cells of dad1 are still filled with liquid at the time of flowering, thus disturbing the dehiscence process. Arabidopsis dehiscent mutants disrupting JA biosynthesis pathway are controlled by several genes such as dde1/opr 3, coil, dad1 and aos/dde2-2 (cited in Yang et al.(2007). The hormone auxin is also involved in this process (Wilson et al., 2011) and auxin synthesized in anthers play a major role in coordinating anther dehiscence, pollen maturation and pre-anthesis filament elongation which are the three factors contributing to successful pollination and anthesis (Cecchetti et al., 2008). Effect of auxin begin in anthers at the end of meiosis stage and at bilocular stage in somatic tissues that are involved in the first step of dehiscence in the microspores. Male sterility in A. thaliana with respect to non-dehiscence of anthers Dehiscence of anthers is a two-step procedure where the lytic opening of stomium is followed by the retraction of the anther wall. The second layer of the anther wall, which is the endothecium, generate forces needed here by swelling and rupturing stomium and then by desiccation that cause differential shrinking of thickened and non-thickened parts of the cell wall. This will result in the outward bending force that retracts the anther wall and cause anther opening. The ms35 mutant of the MYB26 gene fails to produce this secondary thickening and thereby prevent pollen dehiscence. When the pollen from mutant plant was released mechanically from the anther, they were able to fertilize indicating their viability. The breaking of septum and stomium occur normally and the pattern of water movement is also normal. However, the lignified secondary wall thickening in endothelial cells do not happen and thus the shrinkage normally involved with anther wall retraction does not happen. Hence it was obvious that the sterility observed in the male sterile mutant plant was due to a defect in the anther dehiscence process which prevent pollen release. The ms35 mutant has resulted due to a deletion and rearrangement of 1288bp upstream of the translational start of MYB26 which result in the down regulation of MYB26 expression and dehiscence failure (Steiner-Lange et al., 2003) (figure 3).This mutant is different from JA dehiscence mutant. Figure 3. Structure of the MYB26 Gene. (Ref. Yang et al., 2007) The ms35 mutant is the loss-of-function mutant of MYB26 gene. When an A. thaliana population was mutagenized with Zea mays transposon En-1/Spm, a male sterile mutant with a defect in the process of anther dehiscence was formed (Steiner-Langer et al., 2003). This mutation was a result of a transposon insertion in AtMYB26 and is limited only to the inflorescence. The disruption of the DNA binding domain of this R2R3-type MYB transcription factor, resulted in the prevention of the secondary wall thickening of endothecium (Steiner-Lange et el., 2003). Over expression of MYB26 results in ectopic secondary thickening and lignifications of various organs and cell types and over expression of NST1 and NST2 induce ectopic secondary thickening of anther tissues (Mitsuda et al., 2005). As described by Yang et al.(2007), MYB26 may either regulate the genes associated with secondary thickening in the endothecium or function in specifying cell competence and determine which cells undergo secondary thickening. Thevenin et al. (2011) has revealed that repression of two enzymes, CCR (cinnamoyl CoA reductase) and CAD (cinnamoyl alcohol dehydrogenase) are associated with the lignin biosynthetic pathway and thereby cause male sterility in Arabidopsis. There are several dehiscence mutants in Arabidopsis, that involve with the disruption of jasmonic acid (JA) biosynthesis and signaling pathways. A male sterile mutant dad1was identified in A. thaliana by Ishiguro et al. (2001) which was defective in biosynthesis of Jasmonic acid. Anther dehiscence was failed simultaneously with flower opening, lack of maturation of pollen grains and delayed development of flower buds. All defects of dad1 were rescued by application of linoleic acid, which is the initial step of JA biosynthesis. Importance of MYB26 and its ms35 mutant Hybrid plant breeding is an important activity in producing plants with superior growth rate and high yield. Hybrid plants can be produced by effective control of male fertility. A major requirement in hybrid breeding is the control of pollen release so as to prevent self-fertilization. Emasculation by hand is the generally practiced method to remove the male portion of a plant but is a tedious and expensive process. However, correct understanding of the anther and pollen development procedure and mechanism of pollen release, is key to the successful application of male sterility in plant breeding systems and finding efficient methods of hybrid production. Male sterile mutants, either due to lack of viable pollen formation or due to lack of pollen release/dehisce mechanisms are thus valuable in plants where hybrid development are desired. Defects in pollen dehiscence or non-dehiscence of viable pollen have a further advantage as such pollen could be collected and subsequently used for hybrid production. As this is the case with A. thaliana AtMYB26, it is an important manipulating tool of male fertility in higher plants (Steiner-Lange et al, 2003; Wilson et al., 2011). Ability to regulate secondary cell wall thickening in a conserved manner has a significant commercial application for wood and paper industry (Yang et al., 2007). Since secondary cell wall synthesis is regulated by MYB26 gene through NST1 and NST2 genes (Steiner-Lange et al., 2003; Yang et al., 2007), it may be possible that MYB26 also associated with the secondary thickening of xylem tissues which is a result of the expression of NST1 and NST3 genes. Thus, further study of these genes in relation to woody plant species can be valuable in understanding the process of wood formation. Wood is the most abundant biomass produced by plants and it is an important raw material for traditional forest products, paper making and pulping. 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Plant J. 34: 519–528. Tehseen, M., M. Imran, M. Hussain, S. Irum, S. Ali, S. MAnsoor and Y. Zafar (2010) Development of male sterility by silencing Bcp1 gene of Arabidopsis through RNA interference. African J. Biotechnology. 9(19): 2736 - 2741 Thevenin, J., B. Pollet, B. Letarnec, L. Saulnier, L. Gissot, A. M. Grondard, C. Lapierre and L. Jouanin. (2011). The Simultaneous Repression of CCR and CAD, Two Enzymes of the Lignin Biosynthetic Pathway, Results in Sterility and Dwarfism in Arabidopsis thaliana. Mol. Plant. 4:70 - 82 Thompson, E.P., C. Wilkins, V. Demidchik, J.M. Davies and B.J. Glover. (2010). An Arabidopsis flavonoid transporter is required for anther dehiscence and pollen development J Exp Bot. 61(2):439-51. von Malek, B., E. van der Graaff, K. Schneitz and B. Keller (2002). The Arabidopsis male- sterile mutant dde2-2 is defective in the ALLENE OXIDE SYNTHASE gene encoding one of the key enzymes of the jasmonic acid biosynthesis pathway. Planta 216, 187–192. Wilson, Z. A., J. Song, B. Taylor and C. Yang (2011). The final split: the regeneration of anther dehiscence. J. Exp. Bot. 62(5):1633 – 1649 (first published online February 16 2011; accessed 6th May 2011) www.arabidopsis.org. The Arabidopsis Information Resource: Arabidopsis thaliana Yang, C., Z. Xu, J. Song, K. Conner, G. Vizcay Barrena and Z.A. Wilson (2007). Arabidopsis MYB26/MALE STERILE35 regulates secondary thickening in the endothecium and is essential for anther dehiscence, Plant Cell. 19: 534–548. Zhong, R., E. A. Richardson and Z. Ye (2007). The MYB46 transcription factor is a direct target of snd1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell. 19(9): 2776 – 2792 Read More
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