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. 2001 May;183(9):2881-7.
doi: 10.1128/JB.183.9.2881-2887.2001.

Reciprocal regulation of anaerobic and aerobic cell wall mannoprotein gene expression in Saccharomyces cerevisiae

N Abramova  1 , O Sertil, S Mehta, C V Lowry
Affiliations

Reciprocal regulation of anaerobic and aerobic cell wall mannoprotein gene expression in Saccharomyces cerevisiae

N Abramova et al. J Bacteriol. 2001 May.

Abstract

The DAN/TIR genes encode nine cell wall mannoproteins in Saccharomyces cerevisiae which are expressed during anaerobiosis (DAN1, DAN2, DAN3, DAN4, TIR1, TIR2, TIR3, TIR4, and TIP1). Most are expressed within an hour of an anaerobic shift, but DAN2 and DAN3 are expressed after about 3 h. At the same time, CWP1 and CWP2, the genes encoding the major mannoproteins, are down-regulated, suggesting that there is a programmed remodeling of the cell wall in which Cwp1 and Cwp2 are replaced by nine anaerobic counterparts. TIP1, TIR1, TIR2, and TIR4 are also induced during cold shock. Correspondingly, CWP1 is down-regulated during cold shock. As reported elsewhere, Mox4 is a heme-inhibited activator, and Mot3 is a heme-induced repressor of the DAN/TIR genes (but not of TIP1). We show that CWP2 (but not CWP1) is controlled by the same factors, but in reverse fashion-primarily by Mot3 (which can function as either an activator or repressor) but also by Mox4, accounting for the reciprocal regulation of the two groups of genes. Disruptions of TIR1, TIR3, or TIR4 prevent anaerobic growth, indicating that each protein is essential for anaerobic adaptation. The Dan/Tir and Cwp proteins are homologous, with the greatest similarities shown within three subgroups: the Dan proteins, the Tip and Tir proteins, and, more distantly, the Cwp proteins. The clustering of homology corresponds to differences in expression: the Tip and Tir proteins are expressed during hypoxia and cold shock, the Dan proteins are more stringently repressed by oxygen and insensitive to cold shock, and the Cwp proteins are oppositely regulated by oxygen and temperature.

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Figures

FIG. 1
FIG. 1
Homology tree for mannoprotein genes. Puzzle_4 software was used to deduce homology relationships among the DAN/TIR and CWP genes.
FIG. 2
FIG. 2
Expression of DAN/TIR and CWP genes during anaerobic growth. (A) Cells of strain FY23 were grown under aerobic or anaerobic conditions as described in the text and harvested for RNA extraction at the intervals indicated. Northern blots were probed with DAN1, DAN2, DAN3, DAN4, TIR1, TIR3, TIR4, TIP1, and ACT1 as a loading control. (B) The RNA samples used for panel A were probed with CWP1 and CWP2. (C) Cells of strain RZ53 were grown in YPD under aerobic conditions or under anaerobic conditions with and without supplementation by heme (25 μg/ml). The Northern blot was probed with TIR4 and TIR1.
FIG. 3
FIG. 3
Regulation of mannoprotein gene expression during cold shock. Cells of strain FY23 were subjected to cold shock as described in Materials and Methods and harvested for RNA extraction. (A) Northern blots were probed with TIP1, TIR1, and TIR4. (B) Cells of strain FY23 and FY23mox4Δ were grown under aerobic conditions, under anaerobic conditions, or at 13°C. A Northern blot was probed with CWP1. (C) The same blot was probed with TIR4. (D) Cells subjected to cold shock at different temperatures were harvested for RNA extraction. Northern blots were probed with TIP1 and CWP1.
FIG. 4
FIG. 4
Growth of strains carrying disruptions of TIR genes. Strains FY23, FY23tir1Δ, FY23tir3Δ, and FY23tir4Δ transformed with the indicated plasmids were grown under aerobic and anaerobic conditions on SDET-ura plates.
FIG. 5
FIG. 5
Electron microscopy images of cell walls in anaerobic cells. Cells of strain FY23 (A) and FY23tir3Δ (B) were grown in an anaerobic jar for 36 h and processed for electron microscopy as described in Materials and Methods.
FIG. 6
FIG. 6
Regulatory factors controlling expression of CWP1 and CWP2. (A) Cells of strains FY23, FY23mot3Δ, and FY23tup1Δssn6Δ were grown in YPD under aerobic and anaerobic conditions and harvested for RNA extraction. Northern blots were probed with CWP1, CWP2, and ACT1. Phosphorimager data (in arbitrary units) for relative intensities are shown at the bottom. (B) Cells of strains FY23 and FY23mox4Δ were grown under anaerobic conditions in YPD. Phosphorimager data are shown. (C) Cells of strain FY23 carrying YCpGAL1/MOX4 or the YCplac33 vector were grown at 30°C for 4 h under aerobic conditions in SC-galactose-raffinose medium (1) and harvested for RNA extraction. Data from an autoradiographic scan are shown.
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