Nuclear Gene Affecting Greening in Virescent Peanut Leaves

Benedict, C. R.; Ketring, D. L.

doi:10.1104/pp.49.6.972

Cited by 30 publications

(27 citation statements)

References 24 publications

(16 reference statements)

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“…Virescence is quite prevalent in higher plants and has long fascinated plant biologists. Early work has identified virescent mutants from many plant species including maize, cotton, tobacco, peanut, and bean, and genetic analyses have shown that both nuclear and chloroplast mutations can be responsible for the virescent phenotype (5)(6)(7)(8)(9).…”

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confidence: 99%

A Putative Chloroplast Thylakoid Metalloprotease VIRESCENT3 Regulates Chloroplast Development in Arabidopsis thaliana

Qi¹,

Liu²,

Liang

et al. 2016

Journal of Biological Chemistry

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The chloroplast is the site of photosynthesis and many other essential plant metabolic processes, and chloroplast development is an integral part of plant growth and development. Mutants defective in chloroplast development can display various color phenotypes including the intriguing virescence phenotype, which shows yellow/white coloration at the leaf base and greening toward the leaf tip. Through large scale genetic screens, we identified a series of new virescent mutants including virescent3-1 (vir3-1), vir4-1, and vir5-1 in Arabidopsis thaliana. We showed that VIR3 encodes a putative chloroplast metalloprotease by map-based cloning. Through site-directed mutagenesis, we showed that the conserved histidine 235 residue in the zinc binding motif HEAGH of VIR3 is indispensable for VIR3 accumulation in the chloroplast. The chloroplast localization of VIR3 was confirmed by the transient expression of VIR3-GFP in leaf protoplasts. Furthermore, taking advantage of transgenic lines expressing VIR3-FLAG, we demonstrated that VIR3 is an intrinsic thylakoid membrane protein that mainly resides in the stromal lamellae. Moreover, topology analysis using transgenic lines expressing a dual epitope-tagged VIR3 indicated that both the N and C termini of VIR3 are located in the stroma, and the catalytic domain of VIR3 is probably facing the stroma. Blue native gel analysis indicated that VIR3 is likely present as a monomer or part of a small complex in the thylakoid membrane. This work not only implicates VIR3 as a new factor involved in early chloroplast development but also provides more insight into the roles of chloroplast proteases in chloroplast biogenesis.Chloroplasts not only serve as the site of photosynthesis but also are responsible for the production of many essential metabolites in higher plants. Although a descendant of photosynthetic prokaryotic organisms through endosymbiosis, the chloroplast has evolved many unique features including complex regulatory networks to achieve the coordinated expressions of plastid genome and nuclear genome and the coordination of chloroplast development with leaf development (1, 2). Given the importance of the chloroplast, much research has been directed at dissecting the intricate pathways that regulate chloroplast development. One fruitful way has been the identification of mutants that are defective in nuclear genes for chloroplast proteins. Large scale genetic screens have revealed that mutants of nuclear genes for chloroplast proteins can give rise to myriads of visible leaf color phenotypes ranging from albino, yellow, and pale green to virescence and variegation (3).Among the many types of mutants that are associated with chloroplast defects are the intriguing virescent mutants. These mutants display young and emerging tissues that are deficient of photosynthetic pigments, a sign that is often associated with underdeveloped plastids (2, 4). As leaves expand, however, these tissues gradually become greener along the leaf proximaldistal axis. At the whole plant level, the ce...

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confidence: 99%

A Putative Chloroplast Thylakoid Metalloprotease VIRESCENT3 Regulates Chloroplast Development in Arabidopsis thaliana

Qi¹,

Liu²,

Liang

et al. 2016

Journal of Biological Chemistry

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“…Clearly, the mutation of this gene has pleiotropic affects. The mutation induces a lag period in Chl synthesis in the light, possibly by nuclear gene regulation of cytoplasmic events during this period (2). A kinetic analysis of the development of chloroplast and nonchloroplast components in greening mutant and wild type leaves should give insight as to the nature of the mutation.…”

Section: Discussionmentioning

confidence: 99%

“…The mutation of a nuclear gene in peanut seedlings leads to a reduction in the light-induced development of chloroplast fine structure, soluble protein, ribulose-l ,5-diP carboxylase, NADP-glyceraldehyde-3-P dehydrogenase, fructose-1 ,6-diP aldolase, glycerate-3-P kinase, phosphoenolpyruvate carboxylase, and malate dehydrogenase in the primary leaves during the lag phase of Chl synthesis (2). Clearly, the mutation of this gene has pleiotropic affects.…”

Section: Discussionmentioning

confidence: 99%

Elimination of the Lag Period in Chloroplast Development in a Chlorophyll Mutant of Peanuts

1974

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The mutation of a nuclear gene in peanut (Arachis hypogaea L.) plants results in a reduced light-dependent development of chloroplast fine structure, soluble protein, ribulose-1, 5-diP carboxylase, NADP-glyceraldehyde-3-P dehydrogenase, fructose-1 ,6-diP aldolase, glycerate-3-P kinase, phosphoenolpyruvate carboxylase, malate dehydrogenase, and dark respiration during the 72-hour lag period of chlorophyll synthesis in dark-grown leaves exposed to continuous light. The mutation has pleiotropic affects. Kinetic analysis shows there is also a 72-hour lag period in the light-dependent development of NADP-glyceraldehyde-3-P dehydrogenase and fructose-1,6-diP aldolase in the mutant leaves, whereas there is no lag in the development of NAD-malate dehydrogenase and dark respiration. (11,13, 17). In this paper, we describe the conditions for eliminating the mutationally induced lag period in chloroplast development in peanut leaves. A dark period, equal in length to the lag period, prior to exposing the darkgrown leaves to continuous illumination, leads to potentiation.These data implicate nuclear genes in the regulation of the synthesis of constituents (nutrients) required for the early stages of chloroplast development in the dark. MATERIALS AND METHODSMaterials. D-(-)-3-Phosphoglyceric acid tricyclohexylammonium salt, 3-phosphoglyceric acid phosphokinase, glyceraldehyde-3-P dehydrogenase, D-fructose-1 ,6-diP tetracyclohexylammonium salt, NADP, NADH, GSH, and ATP were obtained from Sigma Chemical Company.Plant Material. The inheritance of virescent (T-8 11) (mutant) and normal green (NC4-X) (wild type) Virginia peanuts (Arachis hypogaea L.) has been described (4). The virescent phenotype is inherited as a recessive trait. The seeds were dusted with Arasan -50 Red obtained from E. I. duPont de Nemours and Company2 planted in moist vermiculite and placed in a dark room at 28 C for 6 days. The plants were watered daily after 3 days in the dark. After 6 days in the dark, the seedling hypocotyls were 5 cm long, and the primary leaves were 0.5 cm in length.

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“…Machlachlan and Zalik (18) studied the nuclear virescent of barley and observed that maximum pigment levels were reached 2 to 3 d later than in the wild-type barley. In a virescent nuclear mutant of maize (16) (3) and Phaseolus (7). Fewer thylakoids per granum could also be seen in electron micrographs of chloroplasts from the maternally inherited virescent of soybean (20).…”

Section: Discussionmentioning

confidence: 99%

Characterization of a Virescent Chloroplast Mutant of Tobacco

Archer

Bonnett²

1987

Plant Physiol.

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Virescent mutations produce plants in which young leaves have reduced chlorophyll levels but accumulate nearly normal amounts of chlorophyll as they age; they are predominantly nuclear mutations. We describe here a virescent mutation (designated Vir-c) found in a somatic hybrid line derived from Nicotiana tabacum L. and Nicotiana suaveoekns Lehm. This mutation is inherited maternally. Young, half-expanded Vir-c leaves contained three to six times less chlorophyll than did control leaves, and reached maximum chlorophyll levels much later in development. Chlorophyll synthesis rates and chloroplast numbers per cell in Vir-c were similar to the control, and carotenoid content in Vir-c was sufficient to protect chlorophyll from photo-oxidation. Photosynthetic rates of Vir-c at low light intensities suggested a reduced ability to collect light. Electron micrographs of Vir-c chloroplasts from half-expanded leaves showed a significant reduction in thylakoids per granum. The decrease in granal thylakoids was strongly associated with low chlorophyll levels; mature Vir-c leaves with nearly normal chlorophyll content showed normal granal profiles. These results are discussed in relation to virescent mutants previously described.Virescent mutants are a curious group of higher plants in which young leaves show much reduced Chl content, but recover more levels of Chl as they age. In contrast with many photosynthetic mutations, the virescent mutation is not lethal, and virescent plants survive to flower and produce seed.Virescent mutations occur in a wide range of flowering plants, including tomato (22), maize (6), cotton (5), and peanut (1). Despite the number of virescent mutants that have been described, the primary effect of the mutation is unknown. The phenotype suggests a temporal aberration in some factor governing Chl content, such as the ability to synthesize, protect, or accumulate Chl.The variety of ways Chl content can be influenced may explain why the virescent phenotype is produced by a number of distinct mutant loci within a given species. In maize, for example, 10 mutant loci on 8 different nuclear chromosomes each produce the virescent phenotype. In a few rare instances, virescent mutations have been reported which were maternally inherited. Presumably these were associated with the chloroplast genome (20,26). The existence of both nuclear and cytoplasmic mutations producing the same phenotype supports the view that virescent mutants comprise a diverse group, in which each distinct mutant locus disturbs a specific factor regulating Chl content.

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Nuclear Gene Affecting Greening in Virescent Peanut Leaves

Cited by 30 publications

References 24 publications

A Putative Chloroplast Thylakoid Metalloprotease VIRESCENT3 Regulates Chloroplast Development in Arabidopsis thaliana

A Putative Chloroplast Thylakoid Metalloprotease VIRESCENT3 Regulates Chloroplast Development in Arabidopsis thaliana

Elimination of the Lag Period in Chloroplast Development in a Chlorophyll Mutant of Peanuts

Characterization of a Virescent Chloroplast Mutant of Tobacco

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