The duration of mitosis and daughter cell size are modulated by nutrients in budding yeast

Leitao, Ricardo; Kellogg, Douglas R.

doi:10.1083/jcb.201609114

Cited by 61 publications

(63 citation statements)

References 31 publications

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“…The same samples were probed for the mitotic cyclin Clb2 to provide a marker for mitosis ( Figure 2A). TORC2 activity increased approximately 3-fold in mitosis, which was well-correlated with the previously observed 3-fold increase in growth rate during mitosis ( Figure 2B) (Leitao and Kellogg 2017). The increase in TORC2 activity and growth rate during mitosis was mirrored by an increase in the phosphorylated form of Rts1 ( Figure 2C).…”

Section: Pp2a Rts1 Is Controlled By Ceramide-dependent Signalssupporting

confidence: 71%

“…Thus, cell size is proportional to growth rate, which means that slow growing cells can be nearly half the size of rapidly growing cells (Johnston et al 1977;Fantes and Nurse 1977). Conversely, at least in some cases cell size influences growth rate so that large cells grow faster than small cells (Tzur et al 2009;Sung et al 2013;Schmoller et al 2015;Leitao and Kellogg 2017). Together, these observations show that growth rate is matched to nutrient availability, cell size is matched to growth rate, and growth rate is matched to cell size.…”

Section: Introductionmentioning

confidence: 52%

“…To test these predictions, we took advantage of the fact that the rate of growth varies during the cell cycle. Cells grow slowly during interphase before the rate of growth increases approximately 3-fold as cells enter mitosis (Goranov et al 2009;Leitao and Kellogg 2017). The rapid mitotic growth phase accounts for most of the volume of a budding yeast cell (Leitao and Kellogg 2017).…”

Section: Pp2a Rts1 Is Controlled By Ceramide-dependent Signalsmentioning

confidence: 99%

“…Cells grow slowly during interphase before the rate of growth increases approximately 3-fold as cells enter mitosis (Goranov et al 2009;Leitao and Kellogg 2017). The rapid mitotic growth phase accounts for most of the volume of a budding yeast cell (Leitao and Kellogg 2017). To test whether TORC2 signaling and Rts1 phosphorylation are correlated with growth rate, we used centrifugal elutriation to isolate small cells in early G1 phase and then assayed TORC2 activity and Rts1 phosphorylation as the cells progressed through the cell cycle.…”

Section: Pp2a Rts1 Is Controlled By Ceramide-dependent Signalsmentioning

confidence: 99%

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Modulation of TORC2 Signaling by a Conserved Lkb1 Signaling Axis in Budding Yeast

et al. 2018

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Nutrient availability, growth rate and cell size are closely linked. For example, in budding yeast, the rate of cell growth is proportional to nutrient availability, cell size is proportional to growth rate, and growth rate is proportional to cell size. Thus, cells grow slowly in poor nutrients and are nearly half the size of cells growing in rich nutrients. Moreover, large cells grow faster than small cells. A signaling network that surrounds Tor kinase complex 2 (TORC2) plays an important role in enforcing these proportional relationships. Cells that lack components of the TORC2 network fail to modulate their growth rate or size in response to changes in nutrient availability. Here, we show that budding yeast homologs of the Lkb1 tumor suppressor kinase are required for normal modulation of TORC2 signaling in response to changes in carbon source. Lkb1 kinases activate Snf1/AMPK to initiate transcription of genes required for utilization of poor carbon sources. However, Lkb1 influences TORC2 signaling via a novel pathway that is independent of Snf1/AMPK. Of the three Lkb1 homologs in budding yeast, Elm1 plays the most important role in modulating TORC2. Elm1 activates a pair of related kinases called Gin4 and Hsl1. Previous work found that loss of Gin4 and Hsl1 causes cells to undergo unrestrained growth during a prolonged mitotic arrest, which suggests that they play a role in linking cell cycle progression to cell growth. We found that Gin4 and Hsl1 also control the TORC2 network. In addition, Gin4 and Hsl1 are themselves influenced by signals from the TORC2 network, consistent with previous work showing that the TORC2 network constitutes a feedback loop. Together, the data suggest a model in which the TORC2 network sets growth rate in response to carbon source, while also relaying signals via Gin4 and Hsl1 that set the critical amount of growth required for cell cycle progression. This kind of close linkage between control of cell growth and size would suggest a simple mechanistic explanation for the proportional relationship between cell size and growth rate.3

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Section: Pp2a Rts1 Is Controlled By Ceramide-dependent Signalssupporting

confidence: 71%

Section: Introductionmentioning

confidence: 52%

Section: Pp2a Rts1 Is Controlled By Ceramide-dependent Signalsmentioning

confidence: 99%

Section: Pp2a Rts1 Is Controlled By Ceramide-dependent Signalsmentioning

confidence: 99%

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Modulation of TORC2 Signaling by a Conserved Lkb1 Signaling Axis in Budding Yeast

et al. 2018

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“…Nutrient modulation of cell size also takes place during bud growth and, as we had observed in G1, cell 306 size at birth displays a strong correlation with growth rate at a single cell level during the preceding S-G2-307 M phases (Leitao & Kellogg, 2017). Thus, mechanisms sensing growth rate independently of the specific 308 nutritional conditions also operate during bud volume growth.…”

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confidence: 68%

The chaperone-client network subordinates cell-cycle entry to growth and stress

Moreno

Parisi

Yahya

et al. 2018

Preprint

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14The precise coordination of growth and proliferation has a universal prevalence in cell homeostasis. As a 15 prominent property, cell size is modulated by the coordination between these processes in bacterial, 16 yeast and mammalian cells, but the underlying molecular mechanisms are largely unknown. Here we 17show that multifunctional chaperone systems play a concerted and limiting role in cell-cycle entry, 18 specifically driving nuclear accumulation of the G1 Cdk-cyclin complex. Based on these findings, we 19 establish and test a molecular competition model that recapitulates cell-cycle-entry dependence on 20 growth rate. As key predictions at a single-cell level, we show that availability of the Ydj1 chaperone and 21 nuclear accumulation of the G1 cyclin Cln3 are inversely dependent on growth rate and readily respond 22to changes in protein synthesis and stress conditions that alter protein folding requirements. Thus, 23 chaperone workload would subordinate Start to the biosynthetic machinery and dynamically adjust 24 proliferation to the growth potential of the cell. 25 26

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Organelle size scaling over embryonic development

Wesley

Mishra

Levy

2020

WIREs Developmental Biology

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The duration of mitosis and daughter cell size are modulated by nutrients in budding yeast

Abstract: In budding yeast, cell size is thought to be primarily controlled by a mechanism that delays cell cycle entry until sufficient growth has occurred in G1. Leitao and Kellogg show that nutrients modulate cell size by controlling the amount of growth that occurs during mitosis.

Cited by 61 publications

References 31 publications

Modulation of TORC2 Signaling by a Conserved Lkb1 Signaling Axis in Budding Yeast

Modulation of TORC2 Signaling by a Conserved Lkb1 Signaling Axis in Budding Yeast

The chaperone-client network subordinates cell-cycle entry to growth and stress

Organelle size scaling over embryonic development

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