Identification and characterization of a second plasma membrane H+-ATPase gene subfamily in Nicotiana plumbaginifolia

Moriau, Luc; Bogaerts, Pierre; Jonniaux, Jean-Luc; Boutry, Marc

doi:10.1007/bf00023594

Cited by 56 publications

(60 citation statements)

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“…The deduced amino acid sequence of LHA4 shares 75 to 98% identity with PM H+-ATPases from other plants, with greatest identity to the potato isoform PHA2 (98%) and the N. plumbaginifolia isoform PMA4 (95%). We found that LHA4 groups with the second subfamily of PM H+-ATPase genes, which also includes AHAI, AHA2, AHA3, and PMA4 (Moriau et al, 1993).…”

Section: Discussionmentioning

confidence: 76%

“…The greatest similarity is with the potato isoform PHA2 (98%) and the N. plumbaginifolia isoform PMA4 (95%). Comparisons made over the complete sequences of PM H+-ATPases have led to the suggestion that it is appropriate to differentiate at least two subfamilies within the PM H+-ATPase gene family, with LHA1, PMA1, PMA2, and PMA3 constituting one family, and AHA1, AHA2, AHA3, and PMA4 forming the second family (Moriau et al, 1993). We have extended this analysis to include LHA4 and other recently published sequences (Fig.…”

Section: Sequence Analysismentioning

confidence: 99%

“…Multiple genes encoding PM H+-ATPases have been cloned in tomato (Lycopersicon esculentum; Ewing et al, 1990;Ewing and Bennett, 1994), Nicotiana plumbaginifolia (Boutry et al, 1989;Perez et al, 1992;Moriau et al, 1993), Arabidopsis fhaliana (Harper et al, , 1990(Harper et al, , 1994Pardo and Serrano, 1989;Houlne and Boutry, 1994), potato (Harms et al, 1994), rice (Wada et al, 1992;Ookura et al, 1994), and Vicia faba (L.E. Wimmers, unpublished data).…”

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confidence: 99%

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Sugar Regulates mRNA Abundance of H+-ATPase Gene Family Members in Tomato

1996

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l h e plant plasma membrane H+-ATPase energizes the secondary uptake of nutrients and may facilitate cell expansion by acidifying the cell wall. In yeast, Clc stimulates the accumulation of H+-ATPase mRNA, and the growth rate supported by various sugars is correlated with H+-ATPase protein abundance. Expression of three H+-ATPase genes, LHAI, LHA2, and LHA4, was previously detected in tomato (Lycopersicon esculentum). We have characterized the sequence of the LHA4 gene and examined the expression of these three tomato H+-ATPase genes in growing tissues and i n response to exogenous sugars. LHA4 is a member of the H+-ATPase subfamily, including the Arabidopsis fhaliana genes AHAl, AHA2, and AHA3. l h e 5' untranslated region of the deduced LHA4 cDNA contains a short, open reading frame very similar to that in the Nicofiana plumbaginifolia gene PMAl . LHA4 transcript abundance in seedlings is correlated with cell growth, being 2.5 times greater in hypocotyls of dark-versus light-grown plants. The accumulation of both LHA4 and LHA2 mRNAs is induced by the addition of exogenous sugars and this induction appears to be dependent on sugar uptake and metabolism, because mannitol and 3-Omethylglucose do not stimulate mRNA accumulation. These results suggest that the induction of expression of H+-ATPase genes by metabolizable sugars may be part of a generalized cellular response to increased cell growth and metabolism promoted by the availability of an abundant carbon source.H+-ATPases in the PM plays a critica1 role in the physiology of plants at both the cellular and organismal levels. They establish an electrical potential and pH gradient across the PM, which provides the force for the secondary transport of anions, cations, amino acids, and sugars (Serrano, 1989;Sussman and Harper, 1989). These secondary transport systems control physiological processes such as nutrient uptake by roots, phloem transport, and stomatal function. H+-ATPase in the PM may have other physiological roles, because the enzyme is subjected to control by physiological effectors such as hormones, light, and pathogens (Serrano, 1989;Sussman and Harper, 1989 control of the cell cycle by the regulation of cytosolic pH (Pichon and Desbiez, 1994) and by driving the auxin-induced cell expansion by cell-wall acidification (Rayle and Cleland, 1992). Total H+-ATPase levels in the PM may be directly correlated with growth. Hager et al. (1991) demonstrated by immunodetection that H+-ATPase levels in the PM increased 2-fold during auxin-induced maize coleoptile elongation. Rao et al. (1993) showed that the growth rate of liquid cultures of yeast supported by different sugars is closely correlated with PM H+-ATPase activity. Furthermore, the expression of the primary yeast PM H+-ATPase isoform PMAl was shown to be induced by the addition of growth-inducing exogenous sugars.Considerable progress has recently been made in the understanding of the molecular biology of plant PM H+-ATPases. Multiple genes encoding PM H+-ATPases have been cloned in tomato (Lycopers...

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Section: Discussionmentioning

confidence: 76%

Section: Sequence Analysismentioning

confidence: 99%

mentioning

confidence: 99%

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Sugar Regulates mRNA Abundance of H+-ATPase Gene Family Members in Tomato

1996

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“…The expression vector, pTZ19U-gfp (Duby et al, 2001), contains the PMA4-En50 transcriptional promoter (Zhao et al, 1999), the PMA4 59 untranslated region, BglII, BamHI, and KpnI restriction sites, mGFP4 S65T (Heim et al, 1994;Haseloff et al, 1997), and the nopaline synthase transcription terminator. cDNAs coding for the Nicotiana plumbaginifolia PM H þ -ATPase isoforms PMA2 (Boutry et al, 1989), PMA3 (Boutry et al, 1989), and PMA4 (Moriau et al, 1993) were amplified by PCR to generate a fragment containing appropriate cloning sites at each end. For PMA2, the primer 59-GGGGTACCGGATCCAACAGTGTAT-GATTGCTG-39 was used to remove the stop codon and add a BamHI restriction site (underlined) at the end of the coding sequence from a PMA2 already preceded by a BamHI site (de Kerchove d'Exaerde et al, 1995).…”

Section: Plasmids and Dna Constructsmentioning

confidence: 99%

Targeting of a Nicotiana plumbaginifolia H⁺-ATPase to the Plasma Membrane Is Not by Default and Requires Cytosolic Structural Determinants

et al. 2004

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The structural determinants involved in the targeting of multitransmembrane-span proteins to the plasma membrane (PM) remain poorly understood. The plasma membrane H þ -ATPase (PMA) from Nicotiana plumbaginifolia, a well-characterized 10 transmembrane-span enzyme, was used as a model to identify structural elements essential for targeting to the PM. When PMA2 and PMA4, representatives of the two main PMA subfamilies, were fused to green fluorescent protein (GFP), the chimeras were shown to be still functional and to be correctly and rapidly targeted to the PM in transgenic tobacco. By contrast, chimeric proteins containing various combinations of PMA transmembrane spanning domains accumulated in the Golgi apparatus and not in the PM and displayed slow traffic properties through the secretory pathway. Individual deletion of three of the four cytosolic domains did not prevent PM targeting, but deletion of the large loop or of its nucleotide binding domain resulted in GFP fluorescence accumulating exclusively in the endoplasmic reticulum. The results show that, at least for this polytopic protein, the PM is not the default pathway and that, in contrast with single-pass membrane proteins, cytosolic structural determinants are required for correct targeting.

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“…The two regions flanking this domain, from which the Fl and F2 oligonucleotides were derived, show 100% conservation among the cloned plant H + -ATPases, but the sequences of these domains were not determined for LHA3 through LHA7. Comparisons made over the complete sequences of plant H + -ATPases have led to the suggestion that it is appropriate to differentiate two subfamilies within the H + -ATPase gene family, with LHAl and PMA1, PMA2, and PMA3 constituting one group, and PMA4 and AHA1, AHA2, and AHA3 forming a second group (Moriau et al, 1993). Examination of the limited 69-amino acid region determined for LHAl through LHA7suggests that LHAl and LHAl belong to the first subfamily, since they are identical to PMA1, PMA2, and PMA3 over this region, and that LHA4 belongs to the second subfamily, since it is identical to PMA4, AHA1, and AHA2 and differs by one amino acid from AHA3.…”

Section: Sequence Analysismentioning

confidence: 99%

Assessment of the Number and Expression of P-Type H+-ATPase Genes in Tomato

Ewing

Bennett

1994

Plant Physiol.

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Seven genomic fragments encoding isoforms of tomato (Lycopersicon esculentum) plasma membrane H+-ATPase were cloned and characterized. Genomic DNA gel-blot analysis indicated that probes corresponding to LHAl through LHA7 hybridized to a common set of seven to nine restriction fragments at moderate stringency and to single, distinct fragments at high stringency. RNA gel-blot and polymerase chain reaction (PCR)-based RNA analyses indicated that LHA1, LHA2, and LHA4 transcripts were present in all organs examined (roots, hypocotyls, stems, immature leaves, mature leaves, green fruit, and red ripe fruit). LHAl mRNA was present at similar abundance in all organs, LHA2 mRNA was most abundant in hypocotyls and leaves, and LHA4 mRNA was most abundant in roots and hypocotyls. RNA gel-blot and RNAbased PCR assays indicated that lHA3, lHA.5, LHA6, and LHA7 mRNA was present at very low or nondetectable levels in all organs, suggesting that these genes are either expressed at very low levels or in organs not examined or that they are regulated by hormonal or environmental cues that were not tested. Indoleacetic acid (IAA) treatment of tomato hypocotyl segments resulted in modest changes in abundance of LHA1, LHA2, and LHA4 transcripts, but these changes were not correlated with the time course of IAAinduced growth. In addition, constitutively silent LHA genes were not activated by IAA. These results indicate that at least seven genomic sequences are present in tomato that may encode plasma membrane H+-ATPases, at least three of which are expressed relatively abundantly at the mRNA level.The enzyme primarily responsible for active transport in plants is the plasma membrane H+-ATPase. It is a member of an evolutionarily related family of cation-translocating ATPases that includes the Ca2+-ATPases of plants and animals, the plasma membrane H+-ATPase of fungi, and the Na+,K+-ATPase of animals. This family of P-type ATPases is characterized by formation of a phosphorylated intermediate, inhibition by vanadate, and structural similarity in several conserved domains (Serrano, 1989). The activity of the H+-ATPase generates an electrochemical gradient across the plant cell plasma membrane that drives a number of secondary transport systems, includmg those responsible for the translocation of cations, anions, amino acids, sugars, and hormones (Poole, 1978;Reinhold and Kaplan, 1984). The activity of the H+-ATPase also contributes to the maintenance of intracellular and extracellular pH (Smith and Raven, 1979).

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Identification and characterization of a second plasma membrane H+-ATPase gene subfamily in Nicotiana plumbaginifolia

Cited by 56 publications

References 20 publications

Sugar Regulates mRNA Abundance of H+-ATPase Gene Family Members in Tomato

Sugar Regulates mRNA Abundance of H+-ATPase Gene Family Members in Tomato

Targeting of a Nicotiana plumbaginifolia H⁺-ATPase to the Plasma Membrane Is Not by Default and Requires Cytosolic Structural Determinants

Assessment of the Number and Expression of P-Type H+-ATPase Genes in Tomato

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Identification and characterization of a second plasma membrane H+-ATPase gene subfamily in Nicotiana plumbaginifolia

Cited by 56 publications

References 20 publications

Sugar Regulates mRNA Abundance of H+-ATPase Gene Family Members in Tomato

Sugar Regulates mRNA Abundance of H+-ATPase Gene Family Members in Tomato

Targeting of a Nicotiana plumbaginifolia H+-ATPase to the Plasma Membrane Is Not by Default and Requires Cytosolic Structural Determinants

Assessment of the Number and Expression of P-Type H+-ATPase Genes in Tomato

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Targeting of a Nicotiana plumbaginifolia H⁺-ATPase to the Plasma Membrane Is Not by Default and Requires Cytosolic Structural Determinants