Journal of Experimental Botany, Vol. 53, No. 378, pp. 2143-2149,
November 1, 2002
© 2002 Oxford University Press
KNAP2, a class I KN1-like gene is a negative marker of bud growth potential in apple trees (Malus domestica [L.] Borkh.)
Received 7 June 2002; Accepted 21 June 2002
1 INH, UMR SAGAH A462, 2, rue Le Nôtre, F-49045 Angers Cedex 01, France
2 UFR Sciences, UMR SAGAH A462, Laboratoire ‘Morphogenèse des Ligneux’, 2, boulevard Lavoisier, F-49045 Angers Cedex 01, France
3 UFR Sciences, UMR PAVE A77, Laboratoire de Microbiologie Végétale, 2, boulevard Lavoisier, F-49045 Angers Cedex 01, France
Abbreviations: DIG, digoxigenin; FAA, formaldehyde alcohol acetic acid; PFA, paraformaldehyde; RT-PCR, reverse transcription-polymerase chain reaction.
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
The determinism of bud bursting pattern along the 1-year-old shoot was studied at the molecular and morphological levels in the apple tree variety ‘Lodi’ which shows an acrotonic tendency. At the molecular level, the expression of KNAP2, which belongs to the class I KN1-like gene family, was studied. Measurements were carried out during dormancy (October), breaking dormancy (January) and just before bud bursting (March). The results showed that KNAP2 is more highly expressed in buds that will remain at rest in the spring. Expression of KNAP2 was found in the meristem and in the marginal meristem of the two latest shaped primordia. In the January and March buds, this gene is also expressed in the procambial zone underneath the apical meristem. This study therefore suggests that KNAP2 may be considered as a negative marker of bud growth potential and that the growth inhibition in proximal buds could partially result from differential gene activity. At the morphological level, it was shown that no organogenetic activity took place between October and March as revealed by the constant number of leaf primordia in buds. Nevertheless, those buds likely to grow the following spring had a larger size and fewer hard scales than other buds. This suggests that genetic control may act together with other mechanisms, possibly physical (number of scales) or biochemical, to control bud inhibition.
Key words: Key words: In situ hybridization, KN1-like genes, Malus domestica [L.] Borkh., morphogenesis, vegetative bud.
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
The branching habit of woody plants mainly depends on the way in which 1-year-old shoots ramify, and is therefore linked to the bursting capacity of its buds (Rohde et al., 1997). During the growing season and from initially undifferentiated cells, buds will give rise to new shoots with varying internode and leaf numbers. Axillary buds will be initiated in the axils of leaves later. On leafy shoots of trees, either axillary meristems continue to grow and produce a shoot or they differentiate into a bud and enter dormancy. This latter case is commonly observed in apple trees (Cook et al., 1998). After dormancy, not all of the axillary buds burst and many of them remain latent. When only distal or apical buds burst, this is referred to as acrotony, as opposed to basitony, where axillary buds of a more proximal origin burst and form shoots. To explain the growth potential of each of these buds, Champagnat (1954, 1965) established the concept of a gradient of precedence: this gradient would appear during dormancy and would give advantages to some buds over others without the need for correlative effects between them. However, mechanisms explaining bud-bursting patterns along the 1-year-old shoot are still largely unknown or hypothetical. Therefore, an understanding of the mechanisms which control bud activity and, in particular, meristem activity, constitutes an important question in plant morphogenesis.
Genetic control is thought to be involved in bud growth potential. Measuring gene activity could allow changes to be detected well before cytological changes are visible in the bud and could point to early growth control mechanisms (Canevascini, 1996). Among genes, those involved in the regulation of gene transcription could appear as good markers of bud activity before bud bursting. In this paper, the expression of a KN1-like gene encoding a transcription factor was studied.
KNOTTED1 (KN1), the first homeobox gene found in plants, was isolated from maize plants carrying a dominant mutation that alters leaf development (Vollbrecht et al., 1991). Other plant KN1-like genes have subsequently been isolated in several monocot or herbaceous dicot species (see the review of Chan et al., 1998). For woody species, KN1-like genes have also been identified in Picea abies [L.] Karst. (Sundas-Larsson et al., 1998), pear (Kano-Murakami et al., 1993a) and apple tree (Watillon et al., 1997; Sakamoto et al., 1998). Based on the amino acid sequence and the expression pattern, these KN1-like genes have been classified into two classes (Kerstetter et al., 1994). Most of the class I KN1-like genes are primarily expressed in meristematic vegetative cells and are normally switched off in the predicted position of the incipient leaf in the shoot apical meristem and in mature leaves (Smith et al., 1992; Jackson et al., 1994). Expression patterns in wild, mutant or transgenic plants suggest that the class I KN1-like genes play a role in the maintenance of the shoot apical meristem and in the switch from indeterminate to determinate cell fate (Smith et al., 1992; Sinha et al., 1993; Lincoln et al., 1994; Müller et al., 1995; Dockx et al., 1995; Chuck et al., 1996). In certain cases, the whole plant morphology is deeply altered by abnormal expression of KN1-like genes. For instance, the over-expression of the rice KN1-like gene, OSH1, in tobacco causes abnormal-shaped leaves, but also dwarfism and loss of apical dominance (Kano-Murakami et al., 1993b).
Watillon et al. (1997) have identified two class I KN1-like genes, KNAP1 and KNAP2, in apple trees. No transcripts of these genes were detectable in leaves or floral organs, but expression was detected in elongated parts of the stem that would be associated with meristematic cells in the cambium layer. Sakamoto et al. (1998) isolated a partial sequence of a class I KN1-like gene, named APHB1, and showed that APHB1 is expressed in shoot apical tissues, internodes of elongating shoots and in flowers, but not in mature leaves nor in developing fruits. No study of class I KN1-like genes has been reported so far in vegetative buds during dormancy in apple trees. Given the expression features of class I KN1-like genes and their potential role in morphogenesis it would be of great interest to determine their expression pattern in vegetative buds at different stages and to examine their putative role in the control of bud growth potential.
This question was studied in an acrotonic variety of apple (‘Lodi’) and the expression of KNAP2, a KN1-like gene cloned by Watillon et al. (1997), is reported here in buds along the length of 1-year-old shoots during dormancy (October), breaking dormancy (January) and just before bud bursting (March). These results are discussed with reference to the morphogenetic activity of these buds which was measured during the same period, using a structural approach.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Plant material
Apple (Malus domestica [L.] Borkh.) variety ‘Lodi’ was provided by INRA (Unité d’Amélioration des Espèces Fruitières et Ornementales, Angers, France). Plants were grafted on M.106 in April 1998 and grown under natural conditions in 4.0 l pots containing 80% (v/v) peat and 20% (v/v) perlite. Fertilizers (Osmocote, 7.5 g, Scotts Europe, Holland) were applied 4 weeks after potting and the plants were watered regularly. Buds were collected during two consecutive years (October 1998 to March 1999 and October 1999 to March 2000) according to their position along the shoot formed the previous summer: distal, median and proximal in mid-October (bud dormancy), January (breaking dormancy of buds) and March (just before bud bursting). About five buds per position were excised from the same shoot. Four to five buds between the defined positions were left on the shoot. For RNA extraction, buds were immediately frozen in liquid N2, and stored at –80 °C.
Morphology of axillary vegetative buds
Lengths of axillary buds were measured on the shoot prior to dissection under a stereo-microscope (40x). For each bud, the number of hard scales (external scales), downy scales (internal scales) and leaf primordia was recorded. Statistical analysis was performed using the Instat software and the non-parametric Mann–Witney test.
Total RNA isolation
Total RNA was isolated from buds (200 mg fresh weight, about 20–30 buds) or from leaves using the Ribomag kit (Fisher Scientific, Elancourt, France) following the manufacturer’s instructions.
Cloning probes for RNA analyses
A 230 nt probe of KNAP2 gene was amplified from bud total RNA using RT-PCR.The following primers: sense primer: 5'-GTT GTTCATCAGCTACAGCAT-3'; antisense primer: 5'-CTTGAA GTTCCTGAAGATCGC-3' were designed from the KNAP2 sequence (Watillon et al., 1997), between positions 713 and 943. Five hundred ng of total RNA extracted from buds sampled in February were reverse-transcribed for 1 h at 42 °C with 200 U of M-MLV Reverse transcriptase (Promega, Madison, WI, USA) after oligodT priming. PCR was carried out and the resulting 230 bp DNA fragment was cloned into the pGEM-T vector as described above. Sequence alignment of KNAP2 probe with KNAP1, and other KNOX genes is given Fig. 1. Since KNAP2 probe has a 95% homology with KNAP1 corresponding sequence, transcripts of both KNAP1 and KNAP2 genes will be detected on Northern and in situ experiments.
|
The gene encoding ubiquitin which is commonly used as a positive control in in situ hybridizations (Jackson et al., 1994) was included in this study to verify retention and accessibility of RNA to the probe for in situ hybridization experiments. A 238 nt sequence of the apple ubiquitin gene was cloned using RT-PCR as described above and the following primers: sense primer: 5'-GGT GACGTATGCAGATCTTCG-3'; antisense primer: 5'-ACAACG CAGAGGCACCACCG-3' designed from the sequence of an apple cDNA clone (GenBank Nucleotide Sequence Database accession number MDU 74358).
Northern blotting
Total RNA (20 µg lane–1) from buds or leaves was separated through denaturing formaldehyde gel electrophoresis. Equal loading of each lane was checked through ethidium bromide staining, showing rRNA signals. Northern blotting was then achieved using the NorthernMax kit provided by Ambion (Austin, TX, USA) and following the manufacturer’s instructions. RNA hybridization was carried out using specific antisense RNA probes labelled by in vitro transcription from SP6 RNA polymerase promoter (after linearization of the vector with NcoI) in the presence of [
-32P UTP] (800 Ci mmol–1). After hybridization and washing steps, the filters were exposed to X-ray film at –80 °C.
Preparation of antisense and sense digoxigenin (DIG)-labelled RNA probes for in situ hybridization
Digoxigenin (DIG)-labelled RNA probes were prepared using an in vitro transcription kit (DIG RNA Labeling Kit (SP6/T7), Roche Diagnostics, Mannheim, Germany) according to the manufacturer’s instructions. The antisense and sense probes were transcribed from SP6 or T7 RNA polymerase promoters (after linearization of the vector with NcoI or NotI, respectively). Template DNA was removed by DNase I treatment. DIG-labelled RNA transcripts were precipitated and pellets were resuspended in water at a final concentration of 0.5 µg µl–1.
Tissue preparation and in situ hybridization
Buds were taken from the proximal position of shoots in October, January and March. Hard scales and downy scales were removed to improve fixation. Tissue samples were immediately fixed in FAA solution (3.7% (v/v) formaldehyde, 50% (v/v) ethanol, 5% (v/v) acetic acid) at 4 °C as reported earlier (Brunel, 2001). Fixed tissues were then dehydrated through a graded series of ethanol. The solvent was progressively exchanged with HistoClear II (National Diagnostics, Atlanta, GA, USA), and then tissues were embedded in paraffin (Paraplast, Oxford Labware, St Louis, MO, USA). Samples were cut longitudinally to 8–10 µm sections, mounted on SuperFrost Plus slides (Fischer Scientific, Elancourt, France) and dried at 50 °C overnight. Paraffin was removed through two baths (10 min each) of HistoClear II. Slides were progressively rehydrated in an ethanol series and then washed for 5 min in PBS 1X. Slides were treated with proteinase K at 10 µg ml–1 in PBS 1X for 15 min at 37 °C then incubated in glycine at 2 mg ml–1 in PBS 1X for 5 min at room temperature and washed in PBS 1X. Slides were fixed in PBS 1X containing 4% PFA for 10 min, rinsed in PBS 1X and then acetylated using 10% (v/v) glacial acetic acid in water for 30 s and rinsed in PBS 1X. Before hybridization, slides were dehydrated through a graded ethanol series.
Hybridization, washes and immunodetection of hybridized transcripts were performed as reported earlier (Poupard et al., 2001) using a temperature of 55 °C for hybridization.
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Bursting pattern of Lodi trees, bud structure and morphogenetic activity
The acrotonic tendency of the Lodi trees used in these experiments was checked on 29 1-year-old shoots, untouched during the experimentation. Proximal buds and median buds remained latent in 100% and 55%, respectively, of the 1-year-old shoots observed, whereas distal buds always burst and developed into a new shoot (Fig. 2). When median buds burst, they only developed a rosette of leaves, and never produced a shoot.
|
When bud sizes along 1-year-old shoots were compared, the length of both distal and median buds appeared significantly greater than the length of proximal buds. Results are shown in Fig. 3 for buds collected between October 1999 and March 2000. Similar results were obtained the previous year (data not shown). Except for the proximal position, bud size did not significantly change between October and March. Concerning proximal buds, a slight increase in bud size was measured, however, only one year out of two (Fig. 3). Similarly, an absence of morphogenetic activity within buds was observed during the same period. The total number of leaf structures (scales and leaf primordia) within each bud, whatever its position along the axis remained statistically constant from October to March (Fig. 4). Interestingly, only a few leaf primordia (on average, between 2.7 and 4) were present in buds before bursting. It is noteworthy that a significantly greater number of hard scales was found in proximal buds than in distal buds.
|
|
Accumulation patterns of KNAP2 transcripts in apple vegetative buds
Using Northern blot analysis, the evolution of KNAP2 transcripts was examined in vegetative buds during dormancy (October), dormancy breaking (January), immediately prior to bud bursting (March), and according to bud position along the shoot. Typical expression patterns obtained with KNAP2 are shown in Fig. 5. The results show that KNAP2 was expressed in all buds, but not in mature leaves as checked using Northern analysis (Fig. 5), and RT-PCR (data not shown). KNAP2 expression was not stable during the period under study, and increased in intensity, particularly in March, suggesting a resumption of KNAP2 transcription, close to the period of bud bursting. Most strikingly, KNAP2 expression varied greatly according to bud position, and was always lowest in distal buds, i.e. in those buds that will burst in spring. A faint signal was observed in October and January in distal buds. That signal increased in March, but remained significantly lower than those observed in median and proximal buds, which will remain at rest during the growth period (Fig. 5).
|
In situ localization of KNAP2 transcripts
Tissue localization of KNAP2 gene expression during different stages of vegetative bud development was determined by in situ hybridization of digoxigenin labelled RNA probes to bud longitudinal sections. Figure 6 shows the specific accumulation of KNAP2 mRNA in axillary vegetative buds that originated from the proximal position. In the October samples (Fig. 6A), high levels of KNAP2 transcripts were observed in the shoot meristem and in the marginal meristem of the two youngest shaped leaf primordia. No expression was detected in older leaf primordia, nor in the pith. Control sections probed with sense RNA transcripts showed no signal (Fig. 6D). Control sections hybridized with a ubiquitin probe at each seasonal point gave a signal throughout all tissues indicating that the absence of KNAP2 expression in some cells was not due to altered RNA retention or accessibility (Fig. 6E). In buds excised in January (Fig. 6B) and in March (Fig. 6C), expression of KNAP2 was observed in the same organs as in October (meristem and young primordia) and also in the procambial zone.
|
|
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
The aim was to study the expression of genes which may be involved in the control of bud growth potential and therefore in the branching habit of trees. The KNAP2 gene was chosen since it may control early events well before morphological changes are visible in buds.
The results clearly show that a differential expression of the KNAP2 gene does indeed take place in buds, even when no change in morphogenetic activity, as measured by scales and leaf primordia numbers, was detected. Differences in KNAP2 transcript levels were observed as early as October, and were even more pronounced just before bud bursting in March. While the KNAP2 transcript level remained low at this date in distal buds, a strong signal was observed in proximal as well as median buds. Since, as confirmed here, those latter buds always remain latent in the acrotonic variety under study, this may suggest some involvement of the KNAP2 gene in the negative control of bud bursting capacity. The in situ hybridization experiments showed KNAP2 expression in the apical meristem of buds. Since it has long been suggested that KN1-like genes are involved in the maintenance of the undifferentiated state of meristematic cells (Smith et al., 1992), high levels of KNAP2 expression in proximal buds could contribute to impair the differentiation of meristematic cells into leaf primordia and, consequently, bud growth. Although, the molecular cascade of the control of bud bursting remains unknown and the involvement of the KN1-like genes is still hypothetical, KNAP2 appears to be a good marker of bud growth potential in apple tree.
KNAP2 is expressed in several territories in apple vegetative buds
In addition to its expression in the apical meristem, KNAP2 was also shown to be expressed in the marginal meristem of the two latest shaped leaf primordia and in the procambium. Expression of two members of the class I KN1-like gene family in leaf primordia of tomato has also been reported (Hareven et al., 1996; Janssen et al., 1998). Interestingly, in apple leaf primordia, this expression appeared to be short-lived, since, no expression was detected through in situ hybridization of older leaf primordia present in the bud.
In January and March buds, KNAP2 expression was also observed in the procambial zone. These results are in agreement with those of Lincoln et al. (1994) in Arabidopsis, who showed KNAT1 expression in cells adjacent to the differentiating vascular tissue in the shoot apex. The results are also reinforced by those of Watillon et al. (1997) who, through Northern blot experiments, detected an expression of KNAP2 in the stem. These authors hypothesized that such expression might be relevant to the functioning of the cambium cell layer and the subsequent formation of important secondary structures in woody plants.
These results and those in the literature suggest that the KNAP2 gene is involved in several morphogenetic events and if KNAP2 takes part in the control of bud bursting, it may act through all or part of these processes.
Bud growth potential may be partially determined during the growing season
Bud morphological analysis demonstrated that the increased size of distal and median buds was due to a differential development of leaf primordia or cataphylls. Such differences in bud size was observed as early as October, suggesting that the differential development of leaf primordia along the 1-year-old shoot had occurred along the leafy shoot during the previous summer. Therefore, the pattern of bud bursting in March may be at least partially determined during the previous growing season. It is also interesting to note that buds likely to remain latent present more hard scales than buds likely to grow the following spring. Swartz et al. (1984) have shown in apple trees that the removal of bud scales during the onset or end of dormancy could accelerate bud bursting. Abscisic acid contained in scales could be involved in this inhibition. These results and our own observations suggest that hard scales could also contribute, in association with other factors such as a genetic control, in the inhibition of proximal buds. It would be of great interest to test the possibility of an induction of KNAP2 expression by abscisic acid.
In conclusion, bud growth potential in apple is negatively correlated with KNAP2 expression and the abundance of hard scales. No difference in morphogenetic activity, as expressed by the accumulation of more leaf primordia before bursting, can explain the higher potential of distal buds to burst. Further studies, such as the over-expression of KNAP2 in apple trees, should help to determine the involvement of this gene in the control of bud bursting and improve the understanding of mechanisms ranging between genetical and physical (scales), which together may participate in bud inhibition in spring.
|
Acknowledgements |
|---|
Christian Le Morvan is gratefully acknowledged for his technical assistance in the study of bud morphology, as well as Aisling Judge and Carmel O’Neill for checking the English text. Financial support was provided by the Région Pays de La Loire.
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Brunel N. 2001. Etude du déterminisme de la préséance des bourgeons le long du rameau d’un an chez le pommier (Malus domestica [L.] Borkh.): approches morphologique, biochimique et moléculaire. Thèse de Doctorat, Université d’Angers, France.
Canevascini S. 1996. Gene expression in apical meristem. In: Viémont JD, ed. Activité méristématique caulinaire: de la cytologie et de la biologie moléculaire à la morphogenèse. Xème Colloque Groupe d’Etude de l’Arbre, Angers, France, 16–17 April 1996, 28–34.
Champagnat P. 1954. Les corrélations sur le rameau d’un an des végétaux ligneux. Phyton 4, 1–102.
Champagnat P. 1965. Quelques caractères de la ramification du rameau d’un an des végétaux ligneux. 96ème Congrès pomologie, France, 14–17 October 1965, 9–33.
Chan RL, Gago GM, Palena CM, Gonzalez DH. 1998. Homeobox in plant development. Review. Biochimica et Biophysica Acta 1442, 1–19.[Medline]
Chuck G, Lincoln C, Hake S. 1996. KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. The Plant Cell 8, 1277–1289.[Abstract]
Cook NC, Rabe E, Keulemans J, Jacobs G. 1998. The expression of acrotony in deciduous fruit trees: a study of the apple rootstock M.9. Journal of the American Society for Horticultural Science 123, 30–34.
Dockx J, Quadvlieg N, Keutjes G, Kock P, Weisbeek P, Smeekens S. 1995. The homeobox gene atk1 of Arabidopsis thaliana is expressed in the shoot apex of the seedling and in flowers and inflorescence stems of mature plants. Plant Molecular Biology 28, 723–737.[Web of Science][Medline]
Hareven D, Gutfinger T, Parnis A, Eshed Y, Lifschitz E. 1996. The making of a compound leaf: genetic manipulation of leaf architecture in tomato. Cell 84, 735–744.[Web of Science][Medline]
Jackson D, Veit B, Hake S. 1994. Expression of maize knotted1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120, 405–413.[Abstract]
Janssen B-J, Williams A, Chen J-J, Mathern J, Hake S, Sinha N. 1998. Isolation and characterization of two knotted-like homeobox genes from tomato. Plant Molecular Biology 36, 417–425.[Web of Science][Medline]
Kano-Murakami Y, Kusaba S, Fukumoto M. 1993a. Characterization of the Kn-1 homologous gene in Japanese pear. Journal of the Japanese Society for Horticultural Science 62, Supplement 1, 4–5 (in Japanese).
Kano-Murakami Y, Yanai T, Tagiri A, Matsuoka M. 1993b. A rice homeotic gene, OSH1, causes unusual phenotype in transgenic tobacco. FEBS Letters 334, 365–368.[Web of Science][Medline]
Kerstetter R, Vollbrecht E, Lowe B, Veit B, Yamaguchi J, Hake S. 1994. Sequence analysis and expression patterns divide the maize knotted1-like homeobox genes into two classes. The Plant Cell 6, 1877–1887.
Lincoln C, Long J, Yamaguchi J, Serikawa K, Hake S. 1994. A knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. The Plant Cell 6, 1859–1876.
Müller KJ, Romano N, Gerstner O, Garcia-Maoto F, Pozzi C, Salamini F, Rohde W. 1995. The barley Hooded mutation caused by a duplication in a homeobox gene intron. Nature 374, 727–730.[Medline]
Poupard P, Brunel N, Leduc N, Viémont JD, Strullu DG, Simoneau P. 2001. Expression of a Bet v1 homologue gene encoding a PR 10 protein in birch roots: induction by auxin and localization of the transcripts by in situ hybridization. Australian Journal of Plant Physiology 28, 57–63.
Rohde A, Van Montagu M, Inzé D, Boerjan W. 1997. Factors regulating the expression of cell cycle genes in individual buds of Populus. Planta 201, 43–52.
Sakamoto T, Kusaba S, Kano-Murakami Y, Fukumoto M, Iwahori S. 1998. Two different types of homeobox gene exist in apples. Journal of the Japanese Society for Horticultural Science 67, 372–374.
Sinha NR, Williams RE, Hake S. 1993. Overexpression of the maize homeobox gene, Knotted-1, causes a switch from determinate to indeterminate cell fates. Genes and Development 7, 787–795.
Smith LG, Greene B, Veit B, Hake S. 1992. A dominant mutation in the maize homeobox gene, knotted-1, causes its ectopic expression in leaf cells with altered fates. Development 116, 21–30.[Abstract]
Sundas-Larsson A, Svenson M, Liao H, Engström P. 1998. A homeobox gene with potential developmental control function in the meristem of the conifer Picea abies. Proceedings of the National Academy of Sciences, USA 25, 15118–15122.
Swartz HJ, Geyer AS, Powell LE, Lin S-HC. 1984. The role of bud scales in the dormancy of apples. Journal of the American Society for Horticultural Science 109, 745–749.
Vollbrecht E, Veit B, Sinha N, Hake S. 1991. The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature 250, 241–243.
Watillon B, Kettmann R, Boxus P, Burny A. 1997. Knotted1-like homeobox genes are expressed during apple trees (Malus domestica [L.] Borkh) growth and development. Plant Molecular Biology 33, 757–763.[Web of Science][Medline]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  A. Dusotoit-Coucaud, N. Brunel, P. Kongsawadworakul, U. Viboonjun, A. Lacointe, J.-L. Julien, H. Chrestin, and S. Sakr Sucrose importation into laticifers of Hevea brasiliensis, in relation to ethylene stimulation of latex production Ann. Bot., June 30, 2009; (2009) mcp150v1. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. Testone, L. Bruno, E. Condello, A. Chiappetta, A. Bruno, G. Mele, A. Tartarini, L. Spano, A. M. Innocenti, D. Mariotti, et al. Peach [Prunus persica (L.) Batsch] KNOPE1, a class 1 KNOX orthologue to Arabidopsis BREVIPEDICELLUS/KNAT1, is misexpressed during hyperplasia of leaf curl disease J. Exp. Bot., February 5, 2008; (2008) erm317v2. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P.-E. Lauri Differentiation and growth traits associated with acrotony in the apple tree (Malus xdomestica, Rosaceae) Am. J. Botany, August 1, 2007; 94(8): 1273 - 1281. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||