TY - JOUR
T1 - A reflux-and-growth mechanism explains oscillatory patterning of lateral root branching sites
AU - van den Berg, Thea
AU - Yalamanchili, Kavya
AU - de Gernier, Hugues
AU - Santos Teixeira, Joana
AU - Beeckman, Tom
AU - Scheres, Ben
AU - Willemsen, Viola
AU - Ten Tusscher, Kirsten
N1 - Funding Information:
We thank Joop Vermeer for financial support of K.Y., Rutger Hermsen for advice on statistical analysis and Jan Kees van Amerongen for management of computational facilities. T.v.d.B. and K.t.T. were funded by grant no. 864.14.003 of the Dutch Organization for Scientific Research ( Nederlandse Organisatie voor Wetenschappelijk Onderzoek , NWO), H.d.G. and T.B. by a grant G022516N of the Research Foundation - Flanders (FWO), J.S.T. was funded by grant no. 737.016.012 of NWO , and K.Y. is funded by VIDI grant no 864.13.008 of NWO .
Publisher Copyright:
© 2021 Elsevier Inc.
PY - 2021/8/9
Y1 - 2021/8/9
N2 - Modular, repetitive structures are a key component of complex multicellular body plans across the tree of life. Typically, these structures are prepatterned by temporal oscillations in gene expression or signaling. Although a clock-and-wavefront mechanism was identified and plant leaf phyllotaxis arises from a Turing-type patterning for vertebrate somitogenesis and arthropod segmentation, the mechanism underlying lateral root patterning has remained elusive. To resolve this enigma, we combined computational modeling with in planta experiments. Intriguingly, auxin oscillations automatically emerge in our model from the interplay between a reflux-loop-generated auxin loading zone and stem-cell-driven growth dynamics generating periodic cell-size variations. In contrast to the clock-and-wavefront mechanism and Turing patterning, the uncovered mechanism predicts both frequency and spacing of lateral-root-forming sites to positively correlate with root meristem growth. We validate this prediction experimentally. Combined, our model and experimental results support that a reflux-and-growth patterning mechanism underlies lateral root priming.
AB - Modular, repetitive structures are a key component of complex multicellular body plans across the tree of life. Typically, these structures are prepatterned by temporal oscillations in gene expression or signaling. Although a clock-and-wavefront mechanism was identified and plant leaf phyllotaxis arises from a Turing-type patterning for vertebrate somitogenesis and arthropod segmentation, the mechanism underlying lateral root patterning has remained elusive. To resolve this enigma, we combined computational modeling with in planta experiments. Intriguingly, auxin oscillations automatically emerge in our model from the interplay between a reflux-loop-generated auxin loading zone and stem-cell-driven growth dynamics generating periodic cell-size variations. In contrast to the clock-and-wavefront mechanism and Turing patterning, the uncovered mechanism predicts both frequency and spacing of lateral-root-forming sites to positively correlate with root meristem growth. We validate this prediction experimentally. Combined, our model and experimental results support that a reflux-and-growth patterning mechanism underlies lateral root priming.
KW - auxin transport
KW - computational modeling
KW - experimental validation
KW - lateral root priming
KW - oscillatory priming dynamics
KW - periodic developmental patterning
KW - plant root branching
KW - root growth dynamics
UR - http://www.scopus.com/inward/record.url?scp=85111908045&partnerID=8YFLogxK
U2 - 10.1016/j.devcel.2021.07.005
DO - 10.1016/j.devcel.2021.07.005
M3 - Article
C2 - 34343477
SN - 1534-5807
VL - 56
SP - 2176-2191.e10
JO - Developmental Cell
JF - Developmental Cell
IS - 15
ER -