An apical hypoxic niche sets the pace of shoot meristem activity

Daan A. Weits; Alicja B. Kunkowska; Nicholas C. W. Kamps; Katharina M. S. Portz; Niko K. Packbier; Zoe Nemec Venza; Christophe Gaillochet; Jan U. Lohmann; Ole Pedersen; Joost T. Van Dongen; Francesco Licausi

doi:10.1038/s41586-019-1203-6

An apical hypoxic niche sets the pace of shoot meristem activity

Daan A. Weits, Alicja B. Kunkowska, Nicholas C. W. Kamps, Katharina M. S. Portz, Niko K. Packbier, Zoe Nemec Venza, Christophe Gaillochet, Jan U. Lohmann, Ole Pedersen, Joost T. Van Dongen^*, Francesco Licausi

^*Corresponding author for this work

Freshwater Biology

49 Citations (Scopus)

Abstract

Complex multicellular organisms evolved on Earth in an oxygen-rich atmosphere1; their tissues, including stem-cell niches, require continuous oxygen provision for efficient energy metabolism2. Notably, the maintenance of the pluripotent state of animal stem cells requires hypoxic conditions, whereas higher oxygen tension promotes cell differentiation3. Here we demonstrate, using a combination of genetic reporters and in vivo oxygen measurements, that plant shoot meristems develop embedded in a low-oxygen niche, and that hypoxic conditions are required to regulate the production of new leaves. We show that hypoxia localized to the shoot meristem inhibits the proteolysis of an N-degron-pathway4,5 substrate known as LITTLE ZIPPER 2 (ZPR2)—which evolved to control the activity of the class-III homeodomain-leucine zipper transcription factors6–8—and thereby regulates the activity of shoot meristems. Our results reveal oxygen as a diffusible signal that is involved in the control of stem-cell activity in plants grown under aerobic conditions, which suggests that the spatially distinct distribution of oxygen affects plant development. In molecular terms, this signal is translated into transcriptional regulation by the N-degron pathway, thereby linking the control of metabolic activity to the regulation of development in plants.

Original language	English
Journal	Nature
Volume	569
Pages (from-to)	714-717
ISSN	0028-0836
DOIs	https://doi.org/10.1038/s41586-019-1203-6
Publication status	Published - 30 May 2019

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Cite this

@article{38329cd2ae854b6791e301f7c2e0c174,

title = "An apical hypoxic niche sets the pace of shoot meristem activity",

abstract = "Complex multicellular organisms evolved on Earth in an oxygen-rich atmosphere1; their tissues, including stem-cell niches, require continuous oxygen provision for efficient energy metabolism2. Notably, the maintenance of the pluripotent state of animal stem cells requires hypoxic conditions, whereas higher oxygen tension promotes cell differentiation3. Here we demonstrate, using a combination of genetic reporters and in vivo oxygen measurements, that plant shoot meristems develop embedded in a low-oxygen niche, and that hypoxic conditions are required to regulate the production of new leaves. We show that hypoxia localized to the shoot meristem inhibits the proteolysis of an N-degron-pathway4,5 substrate known as LITTLE ZIPPER 2 (ZPR2)—which evolved to control the activity of the class-III homeodomain-leucine zipper transcription factors6–8—and thereby regulates the activity of shoot meristems. Our results reveal oxygen as a diffusible signal that is involved in the control of stem-cell activity in plants grown under aerobic conditions, which suggests that the spatially distinct distribution of oxygen affects plant development. In molecular terms, this signal is translated into transcriptional regulation by the N-degron pathway, thereby linking the control of metabolic activity to the regulation of development in plants.",

author = "Weits, {Daan A.} and Kunkowska, {Alicja B.} and Kamps, {Nicholas C. W.} and Portz, {Katharina M. S.} and Packbier, {Niko K.} and {Nemec Venza}, Zoe and Christophe Gaillochet and Lohmann, {Jan U.} and Ole Pedersen and {Van Dongen}, {Joost T.} and Francesco Licausi",

year = "2019",

month = may,

day = "30",

doi = "10.1038/s41586-019-1203-6",

language = "English",

volume = "569",

pages = "714--717",

journal = "Nature",

issn = "0028-0836",

publisher = "nature publishing group",

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TY - JOUR

T1 - An apical hypoxic niche sets the pace of shoot meristem activity

AU - Weits, Daan A.

AU - Kunkowska, Alicja B.

AU - Kamps, Nicholas C. W.

AU - Portz, Katharina M. S.

AU - Packbier, Niko K.

AU - Nemec Venza, Zoe

AU - Gaillochet, Christophe

AU - Lohmann, Jan U.

AU - Pedersen, Ole

AU - Van Dongen, Joost T.

AU - Licausi, Francesco

PY - 2019/5/30

Y1 - 2019/5/30

N2 - Complex multicellular organisms evolved on Earth in an oxygen-rich atmosphere1; their tissues, including stem-cell niches, require continuous oxygen provision for efficient energy metabolism2. Notably, the maintenance of the pluripotent state of animal stem cells requires hypoxic conditions, whereas higher oxygen tension promotes cell differentiation3. Here we demonstrate, using a combination of genetic reporters and in vivo oxygen measurements, that plant shoot meristems develop embedded in a low-oxygen niche, and that hypoxic conditions are required to regulate the production of new leaves. We show that hypoxia localized to the shoot meristem inhibits the proteolysis of an N-degron-pathway4,5 substrate known as LITTLE ZIPPER 2 (ZPR2)—which evolved to control the activity of the class-III homeodomain-leucine zipper transcription factors6–8—and thereby regulates the activity of shoot meristems. Our results reveal oxygen as a diffusible signal that is involved in the control of stem-cell activity in plants grown under aerobic conditions, which suggests that the spatially distinct distribution of oxygen affects plant development. In molecular terms, this signal is translated into transcriptional regulation by the N-degron pathway, thereby linking the control of metabolic activity to the regulation of development in plants.

AB - Complex multicellular organisms evolved on Earth in an oxygen-rich atmosphere1; their tissues, including stem-cell niches, require continuous oxygen provision for efficient energy metabolism2. Notably, the maintenance of the pluripotent state of animal stem cells requires hypoxic conditions, whereas higher oxygen tension promotes cell differentiation3. Here we demonstrate, using a combination of genetic reporters and in vivo oxygen measurements, that plant shoot meristems develop embedded in a low-oxygen niche, and that hypoxic conditions are required to regulate the production of new leaves. We show that hypoxia localized to the shoot meristem inhibits the proteolysis of an N-degron-pathway4,5 substrate known as LITTLE ZIPPER 2 (ZPR2)—which evolved to control the activity of the class-III homeodomain-leucine zipper transcription factors6–8—and thereby regulates the activity of shoot meristems. Our results reveal oxygen as a diffusible signal that is involved in the control of stem-cell activity in plants grown under aerobic conditions, which suggests that the spatially distinct distribution of oxygen affects plant development. In molecular terms, this signal is translated into transcriptional regulation by the N-degron pathway, thereby linking the control of metabolic activity to the regulation of development in plants.

U2 - 10.1038/s41586-019-1203-6

DO - 10.1038/s41586-019-1203-6

M3 - Letter

C2 - 31092919

SN - 0028-0836

VL - 569

SP - 714

EP - 717

JO - Nature

JF - Nature

ER -