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From signal transduction to autophagy of plant cell organelles: lessons from yeast and mammals and plant-specific features

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Abstract

Autophagy is an evolutionarily conserved intracellular process for the vacuolar degradation of cytoplasmic constituents. The central structures of this pathway are newly formed double-membrane vesicles (autophagosomes) that deliver excess or damaged cell components into the vacuole or lysosome for proteolytic degradation and monomer recycling. Cellular remodeling by autophagy allows organisms to survive extensive phases of nutrient starvation and exposure to abiotic and biotic stress. Autophagy was initially studied by electron microscopy in diverse organisms, followed by molecular and genetic analyses first in yeast and subsequently in mammals and plants. Experimental data demonstrate that the basic principles, mechanisms, and components characterized in yeast are conserved in mammals and plants to a large extent. However, distinct autophagy pathways appear to differ between kingdoms. Even though direct information remains scarce particularly for plants, the picture is emerging that the signal transduction cascades triggering autophagy and the mechanisms of organelle turnover evolved further in higher eukaryotes for optimization of nutrient recycling. Here, we summarize new research data on nitrogen starvation-induced signal transduction and organelle autophagy and integrate this knowledge into plant physiology.

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Abbreviations

AMPK:

AMP-activated protein kinase

ATG:

autophagy

CAT:

catalase

ConcA:

Concanamycin A

Cvt:

cytoplasm-to-vacuole targeting

DEHP:

di-(2-ethylhexyl)phthalate

eIF2:

eukaryotic translation initiation factor-2

ER:

endoplasmic reticulum

FKBP12:

FK506-binding protein 12

GCN2:

general control non-derepressible-2

LBD:

lateral organ boundary domain

3-MA:

3-Methyladenine

mex1:

maltose excess 1 mutant

MIPA:

micropexophagy apparatus

MAPK:

mitogen-activated protein kinase

NLA:

nitrogen limitation adaptation mutant

NLP:

nodule inception-like protein

NR:

nitrate reductase

PAS:

phagophore assembly site/preautophagosomal structure

PCD:

programmed cell death

PTS1:

peroxisome targeting signal type 1

PEX:

peroxin

PI3K:

phosphatidylinositol 3-kinase

PI4P:

phosphatidylinositol 4′-monophosphate

PMP:

peroxisomal membrane protein

RAPTOR:

regulatory associated protein of mTOR

RCB:

Rubisco-containing body

SAV:

senescence-associated vacuole

S6K:

S6 kinase

SNFI:

sucrose non-fermenting kinase 1

SNRK1:

SNF1/AMPK-related kinase

TOR:

target of rapamycin

TORC1/2:

TOR complex 1/2

VPS:

vacuolar protein sorting

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Acknowledgments

We would like to thank Diane Bassham and the autophagy team of the Subramani laboratory (Andreas Till, Jean-Claude Farré, Taras Nazarko, Ravi Manjithaya, and Ronak Lakhani) for critical reading of the manuscript and valuable suggestions. The authors were supported by and acknowledge UiS funding (SR and CL) and funding from the Russian Foundation for Basic Research, grant #10-04-01186 (OV).

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The authors declare that they have no conflict of interest.

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  1. Centre for Organelle Research, University of Stavanger, 4021, Stavanger, Norway

    Sigrun Reumann & Cathrine Lillo

  2. Komarov Botanical Institute, Russian Academy of Sciences, Laboratory of Plant Ecological Physiology, ul. Professora Popova, 2, 197376, St Petersburg, Russia

    Olga Voitsekhovskaja

  3. Centre for Organelle Research (CORE), Faculty of Science and Technology, University of Stavanger, 4021, Stavanger, Norway

    Sigrun Reumann

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  1. Sigrun Reumann
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Reumann, S., Voitsekhovskaja, O. & Lillo, C. From signal transduction to autophagy of plant cell organelles: lessons from yeast and mammals and plant-specific features. Protoplasma 247, 233–256 (2010). https://doi.org/10.1007/s00709-010-0190-0

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