Development

An apical hypoxic niche sets the pace of shoot meristem activity

[a collaborative effort with Daan Weits (SSSA) and Joost van Dongen (RWTH Aachen)]

Complex multicellular organisms evolved on Earth in an oxygen-rich atmosphere; their tissues, including stem-cell niches, require continuous oxygen provision for efficient energy metabolism. Notably, the maintenance of the pluripotent state of animal stem cells requires hypoxic conditions, whereas higher oxygen tension promotes cell differentiation. 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-pathway substrate known as LITTLE ZIPPER 2 (ZPR2)—which evolved to control the activity of the class-III homeodomain-leucine zipper transcription factors—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.

Jasmonate signalling contributes to primary root inhibition upon oxygen deficiency in Arabidopsis thaliana

Plants, including most crops, are intolerant to waterlogging, a stressful condition that limits the oxygen available for roots, thereby inhibiting their growth and functionality. Whether root growth inhibition represents a preventive measure to save energy or is rather a consequence of reduced metabolic rates has yet to be elucidated. In the present study, we gathered evidence for hypoxic repression of root meristem regulators that leads to root growth inhibition. We also explored the contribution of the hormone jasmonic acid (JA) to this process in Arabidopsis thaliana. Analysis of transcriptomic profiles, visualisation of fluorescent reporters and direct hormone quantification confirmed the activation of JA signalling under hypoxia in the roots. Further, root growth assessment in JA-related mutants in aerobic and anaerobic conditions indicated that JA signalling components contribute to active root inhibition under hypoxia. Finally, we show that the oxygen-sensing transcription factor (TF) RAP2.12 can directly induce Jasmonate Zinc-finger proteins (JAZs), repressors of JA signalling, to establish feedback inhibition. In summary, our study sheds new light on active root growth restriction under hypoxic conditions and on the involvement of the JA hormone in this process and its cross talk with the oxygen sensing machinery of higher plants.