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Article ; Online: The myristoylated amino-terminus of an Arabidopsis calcium-dependent protein kinase mediates plasma membrane localization.

Lu, Sheen X / Hrabak, Estelle M

2013 Volume 82, Issue 3, Page(s) 267–278

Abstract: Calcium-dependent protein kinases (CDPK) are a major group of calcium-stimulated kinases found in plants and some protists. Many CDPKs are membrane-associated, presumably because of lipid modifications at their amino termini. We investigated the ... ...

Abstract	Calcium-dependent protein kinases (CDPK) are a major group of calcium-stimulated kinases found in plants and some protists. Many CDPKs are membrane-associated, presumably because of lipid modifications at their amino termini. We investigated the subcellular location and myristoylation of AtCPK5, a member of the Arabidopsis CDPK family. Most AtCPK5 was associated with the plasma membrane as demonstrated by two-phase fractionation of plant microsomes and by in vivo detection of AtCPK5-GFP fusion proteins. AtCPK5 was a substrate for plant N-myristoyltransferase and myristoylation was prevented by converting the glycine at the proposed site of myristate attachment to alanine (G2A). In transgenic plants, a G2A mutation completely abolished AtCPK5 membrane association, indicating that myristoylation was essential for membrane binding. The first sixteen amino acids of AtCPK5 were sufficient to direct plasma membrane localization. In addition, differentially phosphorylated forms of AtCPK5 were detected both in planta and after expression of AtCPK5 in a cell-free plant extract. Our results demonstrate that AtCPK5 is myristoylated at its amino terminus and that myristoylation is required for membrane binding.
MeSH term(s)	Acyltransferases/metabolism ; Arabidopsis/enzymology ; Arabidopsis/genetics ; Arabidopsis/metabolism ; Arabidopsis Proteins/genetics ; Arabidopsis Proteins/metabolism ; Binding Sites/genetics ; Calcium/metabolism ; Calcium-Calmodulin-Dependent Protein Kinases/genetics ; Calcium-Calmodulin-Dependent Protein Kinases/metabolism ; Cell Membrane/enzymology ; Cell Membrane/metabolism ; Green Fluorescent Proteins/genetics ; Green Fluorescent Proteins/metabolism ; Immunoblotting ; Microscopy, Confocal ; Mutation ; Myristic Acid/metabolism ; Phosphorylation ; Plants, Genetically Modified ; Protein Kinases/genetics ; Protein Kinases/metabolism ; Protein Transport
Chemical Substances	Arabidopsis Proteins ; Myristic Acid (0I3V7S25AW) ; Green Fluorescent Proteins (147336-22-9) ; Acyltransferases (EC 2.3.-) ; glycylpeptide N-tetradecanoyltransferase (EC 2.3.1.97) ; Protein Kinases (EC 2.7.-) ; CPK5 protein, Arabidopsis (EC 2.7.11.17) ; Calcium-Calmodulin-Dependent Protein Kinases (EC 2.7.11.17) ; Calcium (SY7Q814VUP)
Language	English
Publishing date	2013-04-23
Publishing country	Netherlands
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	778032-1
ISSN	1573-5028 ; 0167-4412
ISSN (online)	1573-5028
ISSN	0167-4412
DOI	10.1007/s11103-013-0061-0
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Article ; Online: Chromatin remodeling and the circadian clock: Jumonji C-domain containing proteins.

Lu, Sheen X / Tobin, Elaine M

Plant signaling & behavior

2011 Volume 6, Issue 6, Page(s) 810–814

Abstract: Circadian rhythms are a universal way for organisms, ranging from prokaryotes to humans, to maintain coordination with the daily changes of light and temperature. It is known that a functional circadian clock confers enhanced fitness. In both animals and ...

Abstract	Circadian rhythms are a universal way for organisms, ranging from prokaryotes to humans, to maintain coordination with the daily changes of light and temperature. It is known that a functional circadian clock confers enhanced fitness. In both animals and plants, diverse physiological processes are affected by the clock and more than 10% of transcripts show a circadian rhythm. Recent advances in the field have revealed a link between circadian regulated gene expression and dynamic changes in chromatin. Jumonji C (JmjC) domain-containing proteins have been shown to be involved in chromatin remodeling, acting as histone demethylases. The recent discovery that a JmjC-domain containing protein functions as a novel clock component suggests that histone modification has evolved as an important mechanism at the core of the circadian machinery.
MeSH term(s)	Arabidopsis/genetics ; Arabidopsis/physiology ; Chromatin Assembly and Disassembly/genetics ; Circadian Clocks/genetics ; Jumonji Domain-Containing Histone Demethylases/metabolism ; Models, Biological ; Plant Proteins/metabolism
Chemical Substances	Plant Proteins ; Jumonji Domain-Containing Histone Demethylases (EC 1.14.11.-)
Language	English
Publishing date	2011-06-01
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ISSN	1559-2324
ISSN (online)	1559-2324
DOI	10.4161/psb.6.6.15171
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Article ; Online: Pulsed induction of circadian clock genes in Arabidopsis seedlings.

Knowles, Stephen M / Lu, Sheen X / Tobin, Elaine M

Methods in molecular biology (Clifton, N.J.)

2014 Volume 1158, Page(s) 203–208

Abstract: The Alc-inducible system is a simple, yet effective, "gene switch" that can be used to transiently induce gene expression in Arabidopsis. Here we provide a protocol for using the Alc-inducible system to give a pulse in expression of a circadian clock ... ...

Abstract	The Alc-inducible system is a simple, yet effective, "gene switch" that can be used to transiently induce gene expression in Arabidopsis. Here we provide a protocol for using the Alc-inducible system to give a pulse in expression of a circadian clock gene in transgenic seedlings. The line we use as an example harbors an Alc-inducible copy of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene (Alc∷CCA1). Alc∷CCA1 seedlings are grown on solid MS medium and subsequently treated with ethanol vapor. Because the ethanol is quickly absorbed into the medium upon exposure, the seedlings are moved to fresh plates following treatment to avoid continuous induction. After the induction, the seedlings are harvested over a time-course for future total RNA and/or protein extraction that can be used for subsequent gene expression analyses.
MeSH term(s)	Alcohols/pharmacology ; Arabidopsis/genetics ; Arabidopsis Proteins/genetics ; Circadian Clocks/genetics ; Gene Expression Regulation, Plant/drug effects ; Promoter Regions, Genetic ; Seedlings/genetics
Chemical Substances	Alcohols ; Arabidopsis Proteins
Language	English
Publishing date	2014
Publishing country	United States
Document type	Journal Article
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-4939-0700-7_13
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Article: The myristoylated amino-terminus of an Arabidopsis calcium-dependent protein kinase mediates plasma membrane localization

Lu, Sheen X / Hrabak, Estelle M

Plant molecular biology. 2013 June, v. 82, no. 3

2013

Abstract	Calcium-dependent protein kinases (CDPK) are a major group of calcium-stimulated kinases found in plants and some protists. Many CDPKs are membrane-associated, presumably because of lipid modifications at their amino termini. We investigated the subcellular location and myristoylation of AtCPK5, a member of the Arabidopsis CDPK family. Most AtCPK5 was associated with the plasma membrane as demonstrated by two-phase fractionation of plant microsomes and by in vivo detection of AtCPK5-GFP fusion proteins. AtCPK5 was a substrate for plant N-myristoyltransferase and myristoylation was prevented by converting the glycine at the proposed site of myristate attachment to alanine (G2A). In transgenic plants, a G2A mutation completely abolished AtCPK5 membrane association, indicating that myristoylation was essential for membrane binding. The first sixteen amino acids of AtCPK5 were sufficient to direct plasma membrane localization. In addition, differentially phosphorylated forms of AtCPK5 were detected both in planta and after expression of AtCPK5 in a cell-free plant extract. Our results demonstrate that AtCPK5 is myristoylated at its amino terminus and that myristoylation is required for membrane binding.
Keywords	Arabidopsis ; alanine ; fractionation ; lipids ; microsomes ; mutation ; plant extracts ; plasma membrane ; protein kinases ; proteins ; transgenic plants
Language	English
Dates of publication	2013-06
Size	p. 267-278.
Publishing place	Springer-Verlag
Document type	Article
ZDB-ID	778032-1
ISSN	1573-5028 ; 0167-4412
ISSN (online)	1573-5028
ISSN	0167-4412
DOI	10.1007/s11103-013-0061-0
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Article ; Online: Blue Light- and Low Temperature-Regulated COR27 and COR28 Play Roles in the Arabidopsis Circadian Clock.

Li, Xu / Ma, Dingbang / Lu, Sheen X / Hu, Xinyi / Huang, Rongfeng / Liang, Tong / Xu, Tongda / Tobin, Elaine M / Liu, Hongtao

The Plant cell

2016 Volume 28, Issue 11, Page(s) 2755–2769

Abstract: Light and temperature are two key environmental signals that profoundly affect plant growth and development, but underlying molecular mechanisms of how light and temperature signals affect the circadian clock are largely unknown. Here, we report that ... ...

Abstract	Light and temperature are two key environmental signals that profoundly affect plant growth and development, but underlying molecular mechanisms of how light and temperature signals affect the circadian clock are largely unknown. Here, we report that COR27 and COR28 are regulated not only by low temperatures but also by light signals. COR27 and COR28 are negative regulators of freezing tolerance but positive regulators of flowering, possibly representing a trade-off between freezing tolerance and flowering. Furthermore, loss-of-function mutations in COR27 and COR28 result in period lengthening of various circadian output rhythms and affect central clock gene expression. Also, the cor27 cor28 double mutation affects the pace of the circadian clock. Additionally, COR27 and COR28 are direct targets of CCA1, which represses their transcription via chromatin binding. Finally, we report that COR27 and COR28 bind to the chromatin of TOC1 and PRR5 to repress their transcription, suggesting that their effects on rhythms are in part due to their regulation of TOC1 and PRR5 These data demonstrate that blue light and low temperature-regulated COR27 and COR28 regulate the circadian clock as well as freezing tolerance and flowering time.
MeSH term(s)	Arabidopsis/metabolism ; Arabidopsis/physiology ; Arabidopsis/radiation effects ; Arabidopsis Proteins/genetics ; Arabidopsis Proteins/metabolism ; Circadian Clocks/physiology ; Circadian Clocks/radiation effects ; Circadian Rhythm/physiology ; Circadian Rhythm/radiation effects ; Gene Expression Regulation, Plant/physiology ; Gene Expression Regulation, Plant/radiation effects ; Light ; Repressor Proteins/genetics ; Repressor Proteins/metabolism ; Temperature ; Transcription Factors/genetics ; Transcription Factors/metabolism
Chemical Substances	Arabidopsis Proteins ; CCA1 protein, Arabidopsis ; COR27 protein, Arabidopsis ; COR28 protein, Arabidopsis ; PRR5 protein, Arabidopsis ; Repressor Proteins ; TOC1 protein, Arabidopsis ; Transcription Factors
Language	English
Publishing date	2016
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	623171-8
ISSN	1532-298X ; 1040-4651
ISSN (online)	1532-298X
ISSN	1040-4651
DOI	10.1105/tpc.16.00354
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Article: Testing time: can ethanol-induced pulses of proposed oscillator components phase shift rhythms in Arabidopsis?

Knowles, Stephen M / Lu, Sheen X / Tobin, Elaine M

Journal of biological rhythms

2008 Volume 23, Issue 6, Page(s) 463–471

Abstract: Circadian rhythms are generated by endogenous central oscillators that respond to input from the environment and regulate rhythmic outputs. In Arabidopsis, more than a dozen components that affect rhythms have been identified and used to propose models ... ...

Abstract	Circadian rhythms are generated by endogenous central oscillators that respond to input from the environment and regulate rhythmic outputs. In Arabidopsis, more than a dozen components that affect rhythms have been identified and used to propose models of the central oscillator. However, none has been shown to fulfill one of the expected characteristics of an oscillator component: that a pulse of its expression shifts the phase of circadian rhythms. Here we show that a pulse of the proposed oscillator components CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY) causes dramatic phase shifts in rhythms of expression of the circadian reporter CAB2::LUC, as well as of the clock-associated genes TIMING OF CAB EXPRESSION 1 (TOC1) and GIGANTEA (GI). These results demonstrate that pulses of either CCA1 or LHY are capable of resetting the circadian clock. In contrast, a pulse of TOC1 expression did not elicit phase shifts. Control of TOC1 protein level is in part posttranscriptional; thus a pulse of TOC1 protein could be induced only at times when it is already high. Our work also shows that the ethanol-inducible system can be useful for achieving relatively short (<8 h) pulses of gene expression in seedlings.
MeSH term(s)	Arabidopsis/drug effects ; Arabidopsis/genetics ; Arabidopsis/physiology ; Arabidopsis Proteins/genetics ; Arabidopsis Proteins/immunology ; Arabidopsis Proteins/physiology ; Circadian Rhythm/drug effects ; Circadian Rhythm/genetics ; DNA, Plant/biosynthesis ; DNA, Plant/genetics ; Ethanol/pharmacology ; Gene Expression Regulation, Plant/drug effects ; Luminescence ; RNA, Plant/biosynthesis ; RNA, Plant/genetics ; Transcription Factors/genetics
Chemical Substances	Arabidopsis Proteins ; CCA1 protein, Arabidopsis ; DNA, Plant ; RNA, Plant ; TOC1 protein, Arabidopsis ; Transcription Factors ; Ethanol (3K9958V90M)
Language	English
Publishing date	2008-12-05
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	896387-3
ISSN	1552-4531 ; 0748-7304
ISSN (online)	1552-4531
ISSN	0748-7304
DOI	10.1177/0748730408326749
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Zs.A 2872: Show issues

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Article: An Arabidopsis calcium-dependent protein kinase is associated with the endoplasmic reticulum.

Lu, Sheen X / Hrabak, Estelle M

Plant physiology

2002 Volume 128, Issue 3, Page(s) 1008–1021

Abstract: Arabidopsis contains 34 genes that are predicted to encode calcium-dependent protein kinases (CDPKs). CDPK enzymatic activity previously has been detected in many locations in plant cells, including the cytosol, the cytoskeleton, and the membrane ... ...

Abstract	Arabidopsis contains 34 genes that are predicted to encode calcium-dependent protein kinases (CDPKs). CDPK enzymatic activity previously has been detected in many locations in plant cells, including the cytosol, the cytoskeleton, and the membrane fraction. However, little is known about the subcellular locations of individual CDPKs or the mechanisms involved in targeting them to those locations. We investigated the subcellular location of one Arabidopsis CDPK, AtCPK2, in detail. Membrane-associated AtCPK2 did not partition with the plasma membrane in a two-phase system. Sucrose gradient fractionation of microsomes demonstrated that AtCPK2 was associated with the endoplasmic reticulum (ER). AtCPK2 does not contain transmembrane domains or known ER-targeting signals, but does have predicted amino-terminal acylation sites. AtCPK2 was myristoylated in a cell-free extract and myristoylation was prevented by converting the glycine at the proposed site of myristate attachment to alanine (G2A). In plants, the G2A mutation decreased AtCPK2 membrane association by approximately 50%. A recombinant protein, consisting of the first 10 amino acids of AtCPK2 fused to the amino-terminus of beta-glucuronidase, was also targeted to the ER, indicating that the amino terminus of AtCPK2 can specify ER localization of a soluble protein. These results indicate that AtCPK2 is localized to the ER, that myristoylation is likely to be involved in the membrane association of AtCPK2, and that the amino terminal region of AtCPK2 is sufficient for correct membrane targeting.
MeSH term(s)	Animals ; Arabidopsis/enzymology ; Arabidopsis/genetics ; Arabidopsis Proteins/genetics ; Arabidopsis Proteins/metabolism ; Calcium/metabolism ; Calcium-Binding Proteins/genetics ; Calcium-Binding Proteins/metabolism ; Cloning, Molecular ; DNA, Plant/chemistry ; DNA, Plant/genetics ; Endoplasmic Reticulum/enzymology ; Female ; Gene Expression Regulation, Enzymologic ; Gene Expression Regulation, Plant ; Glucuronidase/genetics ; Glucuronidase/metabolism ; Membrane Proteins/genetics ; Membrane Proteins/metabolism ; Molecular Sequence Data ; Mutation ; Myristic Acid/metabolism ; Plant Proteins ; Plants, Genetically Modified ; Protein Kinases/genetics ; Protein Kinases/metabolism ; Rabbits ; Recombinant Fusion Proteins/genetics ; Recombinant Fusion Proteins/metabolism ; Sequence Analysis, DNA
Chemical Substances	ATCDPK2 protein, Arabidopsis ; Arabidopsis Proteins ; Calcium-Binding Proteins ; DNA, Plant ; Membrane Proteins ; Plant Proteins ; Recombinant Fusion Proteins ; Myristic Acid (0I3V7S25AW) ; Protein Kinases (EC 2.7.-) ; Glucuronidase (EC 3.2.1.31) ; Calcium (SY7Q814VUP)
Language	English
Publishing date	2002-03-12
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	208914-2
ISSN	1532-2548 ; 0032-0889
ISSN (online)	1532-2548
ISSN	0032-0889
DOI	10.1104/pp.010770
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Article: CCA1 and ELF3 Interact in the Control of Hypocotyl Length and Flowering Time in Arabidopsis

Lu, Sheen X / Webb, Candace J / Knowles, Stephen M / Kim, Sally H.J / Wang, Zhiyong / Tobin, Elaine M

Plant physiology. 2012 Feb., v. 158, no. 2

2012

Abstract: The circadian clock is an endogenous oscillator with a period of approximately 24 h that allows organisms to anticipate, and respond to, changes in the environment. In Arabidopsis (Arabidopsis thaliana), the circadian clock regulates a wide variety of ... ...

Abstract	The circadian clock is an endogenous oscillator with a period of approximately 24 h that allows organisms to anticipate, and respond to, changes in the environment. In Arabidopsis (Arabidopsis thaliana), the circadian clock regulates a wide variety of physiological processes, including hypocotyl elongation and flowering time. CIRCADIAN CLOCK ASSOCIATED1 (CCA1) is a central clock component, and CCA1 overexpression causes circadian dysfunction, elongated hypocotyls, and late flowering. EARLY FLOWERING3 (ELF3) modulates light input to the clock and is also postulated to be part of the clock mechanism. elf3 mutations cause light-dependent arrhythmicity, elongated hypocotyls, and early flowering. Although both genes affect similar processes, their relationship is not clear. Here, we show that CCA1 represses ELF3 by associating with its promoter, completing a CCA1-ELF3 negative feedback loop that places ELF3 within the oscillator. We also show that ELF3 acts downstream of CCA1, mediating the repression of PHYTOCHROME-INTERACTING FACTOR4 (PIF4) and PIF5 in the control of hypocotyl elongation. In the regulation of flowering, our findings show that ELF3 and CCA1 either cooperate or act in parallel through the CONSTANS/FLOWERING LOCUS T pathway. In addition, we show that CCA1 represses GIGANTEA and SUPPRESSOR OF CONSTANS1 by direct interaction with their promoters, revealing additional connections between the circadian clock and the flowering pathways.
Keywords	Arabidopsis thaliana ; circadian rhythm ; flowering ; genes ; hypocotyls
Language	English
Dates of publication	2012-02
Size	p. 1079-1088.
Publishing place	American Society of Plant Biologists
Document type	Article
ZDB-ID	208914-2
ISSN	1532-2548 ; 0032-0889
ISSN (online)	1532-2548
ISSN	0032-0889
Database	NAL-Catalogue (AGRICOLA)

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Article: CIRCADIAN CLOCK ASSOCIATED1 and LATE ELONGATED HYPOCOTYL Function Synergistically in the Circadian Clock of Arabidopsis

Lu, Sheen X / Knowles, Stephen M / Andronis, Christos / Ong, May S / Tobin, Elaine M

Plant physiology. 2009 June, v. 150, no. 2

2009

Abstract: The circadian clock is an endogenous mechanism that coordinates biological processes with daily and seasonal changes in the environment. Heterodimerization of central clock components is an important way of controlling clock function in several different ...

Abstract	The circadian clock is an endogenous mechanism that coordinates biological processes with daily and seasonal changes in the environment. Heterodimerization of central clock components is an important way of controlling clock function in several different circadian systems. CIRCADIAN CLOCK ASSOCIATED1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY) are Myb-related proteins that function in or close to the central oscillator in Arabidopsis (Arabidopsis thaliana). Single mutants of cca1 and lhy have a phenotype of short-period rhythms. cca1 lhy double mutants show an even shorter period phenotype than the cca1 single mutant, suggesting that CCA1 and LHY are only partially functionally redundant. To determine whether CCA1 and LHY act in parallel or synergistically in the circadian clock, we examined their expression in both light-grown and etiolated seedlings. We have shown that LHY and CCA1 bind to the same region of the promoter of a Light-harvesting chlorophyll a/b protein (Lhcb, also known as CAB). CCA1 and LHY can form homodimers, and they also colocalize in the nucleus and heterodimerize in vitro and in vivo. In Arabidopsis, CCA1 and LHY physically interact in a manner independent of photoperiod. Moreover, results from gel filtration chromatography indicate that CCA1 and LHY are present in the same large complex in plants. Taken together, these results imply that CCA1 and LHY function synergistically in regulating circadian rhythms of Arabidopsis.
Keywords	Arabidopsis thaliana ; chlorophyll ; chromatography ; circadian rhythm ; filtration ; mutants ; phenotype ; photoperiod ; promoter regions ; proteins ; seasonal variation ; seedlings
Language	English
Dates of publication	2009-06
Size	p. 834-843.
Publishing place	American Society of Plant Biologists
Document type	Article
ZDB-ID	208914-2
ISSN	1532-2548 ; 0032-0889
ISSN (online)	1532-2548
ISSN	0032-0889
Database	NAL-Catalogue (AGRICOLA)

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Article: A Role for Protein Kinase Casein Kinase2 α-Subunits in the Arabidopsis Circadian Clock

Lu, Sheen X / Liu, Hongtao / Knowles, Stephen M / Li, Jian / Ma, Ligeng / Tobin, Elaine M / Lin, Chentao

Plant physiology. 2011 Nov., v. 157, no. 3

2011

Abstract: Circadian rhythms are autoregulatory, endogenous rhythms with a period of approximately 24 h. A wide variety of physiological and molecular processes are regulated by the circadian clock in organisms ranging from bacteria to humans. Phosphorylation of ... ...

Abstract	Circadian rhythms are autoregulatory, endogenous rhythms with a period of approximately 24 h. A wide variety of physiological and molecular processes are regulated by the circadian clock in organisms ranging from bacteria to humans. Phosphorylation of clock proteins plays a critical role in generating proper circadian rhythms. Casein Kinase2 (CK2) is an evolutionarily conserved serine/threonine protein kinase composed of two catalytic α-subunits and two regulatory β-subunits. Although most of the molecular components responsible for circadian function are not conserved between kingdoms, CK2 is a well-conserved clock component modulating the stability and subcellular localization of essential clock proteins. Here, we examined the effects of a cka1a2a3 triple mutant on the Arabidopsis (Arabidopsis thaliana) circadian clock. Loss-of-function mutations in three nuclear-localized CK2α subunits result in period lengthening of various circadian output rhythms and central clock gene expression, demonstrating that the cka1a2a3 triple mutant affects the pace of the circadian clock. Additionally, the cka1a2a3 triple mutant has reduced levels of CK2 kinase activity and CIRCADIAN CLOCK ASSOCIATED1 phosphorylation in vitro. Finally, we found that the photoperiodic flowering response, which is regulated by circadian rhythms, was reduced in the cka1a2a3 triple mutant and that the plants flowered later under long-day conditions. These data demonstrate that CK2α subunits are important components of the Arabidopsis circadian system and their effects on rhythms are in part due to their phosphorylation of CIRCADIAN CLOCK ASSOCIATED1.
Keywords	Arabidopsis thaliana ; casein ; circadian rhythm ; enzyme activity ; flowering ; gene expression ; mutants ; mutation ; protein kinases ; protein phosphorylation ; serine ; threonine
Language	English
Dates of publication	2011-11
Size	p. 1537-1545.
Publishing place	American Society of Plant Biologists
Document type	Article
ZDB-ID	208914-2
ISSN	1532-2548 ; 0032-0889
ISSN (online)	1532-2548
ISSN	0032-0889
Database	NAL-Catalogue (AGRICOLA)

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