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Title: Cytokinin signaling localized in phloem noncell‐autonomously regulates cambial activity during secondary growth of Populus stems

Journal Article · · New Phytologist
DOI: https://doi.org/10.1111/nph.17255 · OSTI ID:1779377
 [1];  [1];  [1];  [1]; ORCiD logo [1]; ORCiD logo [2]
  1. Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation School of Life Sciences Southwest University Chongqing 400715 China
  2. Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation School of Life Sciences Southwest University Chongqing 400715 China, Key Laboratory of Eco‐environments of Three Gorges Reservoir Region Ministry of Education School of Life Sciences Southwest University Chongqing 400715 China

Summary The regulation of cytokinin on secondary vascular development has been uncovered by modulating cytokinin content. However, it remains unclear how cytokinin enriched in developing secondary phloem regulates cambium activity in poplar. Here, we visualized the gradient distribution of cytokinin with a peak in the secondary phloem of poplar stem via immunohistochemical imaging, and determined the role of phloem‐located cytokinin signaling during wood formation. We generated transgenic poplar harboring cytokinin oxidase/dehydrogenase ( CKX)2 , a gene encoding a cytokinin degrading enzyme, driven by the phloem‐specific CLE41b promoter, indicating that the disruption of the cytokinin gradient pattern restricts the cambial activity. The RNA interference‐based knockdown of the histidine kinase ( HK ) genes encoding cytokinin receptors specifically in secondary phloem significantly compromised the division activity of cambial cells, whereas the phloem‐specific expression of a type‐B response regulator (RR) transcription factor stimulated cambial proliferation, providing evidence for the noncell‐autonomous regulation of local cytokinin signaling on the cambial activity. Moreover, the cambium‐specific knockdown of HK s also led to restricted cambial activity, and the defects were aggravated by the reduced cytokinin accumulation. Our results showed that local cytokinin signaling in secondary phloem regulates cambial activity noncell‐autonomously, and coordinately with its local signaling in cambium.

Sponsoring Organization:
USDOE
OSTI ID:
1779377
Journal Information:
New Phytologist, Journal Name: New Phytologist Journal Issue: 4 Vol. 230; ISSN 0028-646X
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (62)

The chitinase gene (Bbchit1) from Beauveria bassiana enhances resistance to Cytospora chrysosperma in Populus tomentosa Carr. journal May 2010
ABA and cytokinins: challenge and opportunity for plant stress research journal February 2016
Phloem-Transported Cytokinin Regulates Polar Auxin Transport and Maintains Vascular Pattern in the Root Meristem journal June 2011
Cytokinin Induces Cell Division in the Quiescent Center of the Arabidopsis Root Apical Meristem journal October 2013
Cytokinin and Auxin Display Distinct but Interconnected Distribution and Signaling Profiles to Stimulate Cambial Activity journal August 2016
Cytokinin signaling and transcriptional networks journal October 2010
The formation of wood and its control journal February 2014
Systems genetics of wood formation journal April 2016
How to organize bidirectional tissue production? journal October 2019
Auxin transport inhibitors block PIN1 cycling and vesicle trafficking journal September 2001
Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length journal July 2000
Plant-thickening mechanisms revealed journal January 2019
Stem cell function during plant vascular development journal November 2012
Direct control of shoot meristem activity by a cytokinin-activating enzyme journal February 2007
Spatial specificity of auxin responses coordinates wood formation journal February 2018
WUSCHEL acts as an auxin response rheostat to maintain apical stem cells in Arabidopsis journal November 2019
High levels of auxin signalling define the stem-cell organizer of the vascular cambium journal January 2019
Mobile PEAR transcription factors integrate positional cues to prime cambial growth journal January 2019
The shoot controls zeatin riboside export from pea roots. Evidence from the branching mutant rms4 journal February 1997
Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis : tissue specificity and regulation by auxin, cytokinin, and nitrate journal January 2004
Cytokinin oxidase or dehydrogenase?: Mechanism of cytokinin degradation in cereals journal January 2001
New Insights into the Biology of Cytokinin Degradation journal May 2006
In planta functions of the Arabidopsis cytokinin receptor family journal May 2004
Cytokinin signaling regulates cambial development in poplar journal December 2008
Cytokinins are central regulators of cambial activity journal December 2008
Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem journal August 2009
Auxin as a positional signal in pattern formation in plants. journal August 1996
Identification of Genes Encoding Adenylate Isopentenyltransferase, a Cytokinin Biosynthesis Enzyme, in Arabidopsis thaliana journal April 2001
Arabidopsis CYP735A1 and CYP735A2 Encode Cytokinin Hydroxylases That Catalyze the Biosynthesis of trans-Zeatin journal July 2004
Regulation of vascular cell division journal December 2016
Cytokinin inhibits cotton fiber initiation by disrupting PIN3a-mediated asymmetric accumulation of auxin in the ovule epidermis journal April 2019
Genomic Organization and Evolutionary Conservation of Plant D-Type Cyclins journal October 2007
The Cytokinin Type-B Response Regulator PtRR13 Is a Negative Regulator of Adventitious Root Development in Populus journal April 2009
CHIMERIC FLORAL ORGANS1 , Encoding a Monocot-Specific MADS Box Protein, Regulates Floral Organ Identity in Rice journal August 2012
A Radial Concentration Gradient of Indole-3-Acetic Acid Is Related to Secondary Xylem Development in Hybrid Aspen journal October 1997
Indole-3-Acetic Acid Controls Cambial Growth in Scots Pine by Positional Signaling journal May 1998
Characterization of the Response of the Arabidopsis Response Regulator Gene Family to Cytokinin journal December 2000
Cytokinin-Deficient Transgenic Arabidopsis Plants Show Multiple Developmental Alterations Indicating Opposite Functions of Cytokinins in the Regulation of Shoot and Root Meristem Activity journal October 2003
Two Genes with Similarity to Bacterial Response Regulators Are Rapidly and Specifically Induced by Cytokinin in Arabidopsis journal June 1998
A High-Resolution Transcript Profile across the Wood-Forming Meristem of Poplar Identifies Potential Regulators of Cambial Stem Cell Identity journal August 2004
Dissecting the Molecular Basis of the Regulation of Wood Formation by Auxin in Hybrid Aspen journal April 2008
CENL1 Expression in the Rib Meristem Affects Stem Elongation and the Transition to Dormancy in Populus journal January 2008
Autophagy Negatively Regulates Cell Death by Controlling NPR1-Dependent Salicylic Acid Signaling during Senescence and the Innate Immune Response in Arabidopsis journal September 2009
The Yin-Yang of Hormones: Cytokinin and Auxin Interactions in Plant Development journal January 2015
Type-B ARABIDOPSIS RESPONSE REGULATORs Specify the Shoot Stem Cell Niche by Dual Regulation of WUSCHEL journal June 2017
AspWood: High-Spatial-Resolution Transcriptome Profiles Reveal Uncharacterized Modularity of Wood Formation in Populus tremula journal June 2017
Analyses of GA20ox - and GID1 -over-expressing aspen suggest that gibberellins play two distinct roles in wood formation journal June 2009
Metabolism and Long-distance Translocation of Cytokinins journal January 2010
WUSCHEL ‐ RELATED HOMEOBOX 4 ( WOX 4) ‐like genes regulate cambial cell division activity and secondary growth in Populus trees journal June 2017
MiR319a‐targeted PtoTCP20 regulates secondary growth via interactions with PtoWOX4 and PtoWND6 in Populus tomentosa journal July 2020
A xylem‐produced peptide PtrCLE20 inhibits vascular cambium activity in Populus journal June 2019
Auxin gradients across wood - instructive or incidental? journal December 2013
Cytokinin Oxidase Regulates Rice Grain Production journal July 2005
The Dynamics of Cambial Stem Cell Activity journal April 2019
Cytokinins journal January 2014
Vascular Cambium Development journal January 2015
AINTEGUMENTA and the D-type cyclin CYCD3;1 regulate root secondary growth and respond to cytokinins journal September 2015
Crossing paths: cytokinin signalling and crosstalk journal April 2013
Cellular organisation of the Arabidopsis thaliana root journal September 1993
Embryonic origin of the Arabidopsis primary root and root meristem initials journal September 1994
Bifacial cambium stem cells generate xylem and phloem during radial plant growth journal January 2019
Cytokinin Transporters: Multisite Players in Cytokinin Homeostasis and Signal Distribution journal May 2019