Expression quantitative trait loci mapping identified PtrXB38 as a key hub gene in adventitious root development in Populus

Tao Yao; Jin Zhang; Timothy B. Yates; Him K. Shrestha; Nancy L. Engle; Raphael Ployet; Cai John; Kai Feng; William Patrick Bewg; Margot S.S. Chen; Haiwei Lu; Scott A. Harding; Zhenzhen Qiao; Sara S. Jawdy; Mengjun Shu; Wenya Yuan; Khadijeh Mozaffari; Anne E. Harman-Ware; Renee M. Happs; Larry M. York; Brad M. Binder; Yuko Yoshinaga; Christopher Daum; Timothy J. Tschaplinski; Paul E. Abraham; Chung Jui Tsai; Kerrie Barry; Anna Lipzen; Jeremy Schmutz; Gerald A. Tuskan; Jin Gui Chen; Wellington Muchero

doi:10.1111/nph.19126

Expression quantitative trait loci mapping identified PtrXB38 as a key hub gene in adventitious root development in Populus

Tao Yao, Jin Zhang, Timothy B. Yates, Him K. Shrestha, Nancy L. Engle, Raphael Ployet, Cai John, Kai Feng, William Patrick Bewg, Margot S.S. Chen, Haiwei Lu, Scott A. Harding, Zhenzhen Qiao, Sara S. Jawdy, Mengjun Shu, Wenya Yuan, Khadijeh Mozaffari, Anne E. Harman-Ware, Renee M. Happs, Larry M. YorkBrad M. Binder, Yuko Yoshinaga, Christopher Daum, Timothy J. Tschaplinski, Paul E. Abraham, Chung Jui Tsai, Kerrie Barry, Anna Lipzen, Jeremy Schmutz, Gerald A. Tuskan, Jin Gui Chen, Wellington Muchero

Research output: Contribution to journal › Article › peer-review

6 Scopus citations

Abstract

Plant establishment requires the formation and development of an extensive root system with architecture modulated by complex genetic networks. Here, we report the identification of the PtrXB38 gene as an expression quantitative trait loci (eQTL) hotspot, mapped using 390 leaf and 444 xylem Populus trichocarpa transcriptomes. Among predicted targets of this trans-eQTL were genes involved in plant hormone responses and root development. Overexpression of PtrXB38 in Populus led to significant increases in callusing and formation of both stem-born roots and base-born adventitious roots. Omics studies revealed that genes and proteins controlling auxin transport and signaling were involved in PtrXB38-mediated adventitious root formation. Protein–protein interaction assays indicated that PtrXB38 interacts with components of endosomal sorting complexes required for transport machinery, implying that PtrXB38-regulated root development may be mediated by regulating endocytosis pathway. Taken together, this work identified a crucial root development regulator and sheds light on the discovery of other plant developmental regulators through combining eQTL mapping and omics approaches.

Original language	English
Pages (from-to)	2248-2264
Number of pages	17
Journal	New Phytologist
Volume	239
Issue number	6
DOIs	https://doi.org/10.1111/nph.19126
State	Published - Sep 2023

Funding

We thank Prof. Nam‐Hai Chua from Temasek Life Sciences Laboratory for the gift of MBP‐DC‐MYC vector. We thank Miranda Clark, David McLennan, and Jamie McBrien for growing and maintaining plants in Oak Ridge National Laboratory (ORNL) greenhouses and Crissa Doeppke for biomass characterization assistance at National Renewable Energy Laboratory (NREL). We thank the US Department of Energy Joint Genome Institute and collaborators for prepublication access to the × INRA 717‐1B4 genome sequence and annotation. This research was supported by the BioEnergy Science Center (BESC) and the Center for Bioenergy Innovation (CBI). BESC and CBI are Bioenergy Research Centers supported by the Office of Biological and Environmental Research in the US Department of Energy Office of Science. This research used resources of the Compute and Data Environment for Science (CADES) at ORNL, which is managed by UT‐Battelle, LLC for the Office of Science of the US Department of Energy under Contract no. DE‐AC05‐00OR22725. We are grateful for prepublication access to poplar common garden expression data in leaf and xylem from CBI and the US Department of Energy Joint Genome Institute. The work (proposal: 10.46936/10.25585/60000674 and 10.46936/10.25585/60001013 ) conducted by the US Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, is supported by the Office of Science of the US Department of Energy under Contract No. DE‐AC02‐05CH11231. This research was also supported by the US Department of Energy (DOE), Office of Energy Efficiency and Renewable Energy (EERE), Bioenergy Technologies Office (BETO), under Award No. DE‐AC36‐08GO28308 with NREL. This manuscript has been authored by UT‐Battelle, LLC under Contract No. DE‐AC05‐00OR22725 with the US Department of Energy. The United States Government retains and the publisher, by accepting the article for publication, acknowledges that the United States Government retains a non‐exclusive, paid‐up, irrevocable, worldwide license to publish or reproduce the published form of this manuscript, or allow others to do so, for United States Government purposes. The Department of Energy will provide public access to these results of federally sponsored research in accordance with the DOE Public Access Plan ( http://energy.gov/downloads/doe‐public‐access‐plan ). Populus tremula Populus alba We thank Prof. Nam-Hai Chua from Temasek Life Sciences Laboratory for the gift of MBP-DC-MYC vector. We thank Miranda Clark, David McLennan, and Jamie McBrien for growing and maintaining plants in Oak Ridge National Laboratory (ORNL) greenhouses and Crissa Doeppke for biomass characterization assistance at National Renewable Energy Laboratory (NREL). We thank the US Department of Energy Joint Genome Institute and collaborators for prepublication access to the Populus tremula × Populus alba INRA 717-1B4 genome sequence and annotation. This research was supported by the BioEnergy Science Center (BESC) and the Center for Bioenergy Innovation (CBI). BESC and CBI are Bioenergy Research Centers supported by the Office of Biological and Environmental Research in the US Department of Energy Office of Science. This research used resources of the Compute and Data Environment for Science (CADES) at ORNL, which is managed by UT-Battelle, LLC for the Office of Science of the US Department of Energy under Contract no. DE-AC05-00OR22725. We are grateful for prepublication access to poplar common garden expression data in leaf and xylem from CBI and the US Department of Energy Joint Genome Institute. The work (proposal: 10.46936/10.25585/60000674 and 10.46936/10.25585/60001013) conducted by the US Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, is supported by the Office of Science of the US Department of Energy under Contract No. DE-AC02-05CH11231. This research was also supported by the US Department of Energy (DOE), Office of Energy Efficiency and Renewable Energy (EERE), Bioenergy Technologies Office (BETO), under Award No. DE-AC36-08GO28308 with NREL. This manuscript has been authored by UT-Battelle, LLC under Contract No. DE-AC05-00OR22725 with the US Department of Energy. The United States Government retains and the publisher, by accepting the article for publication, acknowledges that the United States Government retains a non-exclusive, paid-up, irrevocable, worldwide license to publish or reproduce the published form of this manuscript, or allow others to do so, for United States Government purposes. The Department of Energy will provide public access to these results of federally sponsored research in accordance with the DOE Public Access Plan (http://energy.gov/downloads/doe-public-access-plan).

Keywords

Populus
PtrXB38
auxin signaling
developmental regulator
expression quantitative trait loci (eQTLs)
stem-born root formation

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10.1111/nph.19126

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Yao, T., Zhang, J., Yates, T. B., Shrestha, H. K., Engle, N. L., Ployet, R., John, C., Feng, K., Bewg, W. P., Chen, M. S. S., Lu, H., Harding, S. A., Qiao, Z., Jawdy, S. S., Shu, M., Yuan, W., Mozaffari, K., Harman-Ware, A. E., Happs, R. M., ... Muchero, W. (2023). Expression quantitative trait loci mapping identified PtrXB38 as a key hub gene in adventitious root development in Populus. New Phytologist, 239(6), 2248-2264. https://doi.org/10.1111/nph.19126

@article{5af2b55cd40f4c869106324f3c679fee,

title = "Expression quantitative trait loci mapping identified PtrXB38 as a key hub gene in adventitious root development in Populus",

abstract = "Plant establishment requires the formation and development of an extensive root system with architecture modulated by complex genetic networks. Here, we report the identification of the PtrXB38 gene as an expression quantitative trait loci (eQTL) hotspot, mapped using 390 leaf and 444 xylem Populus trichocarpa transcriptomes. Among predicted targets of this trans-eQTL were genes involved in plant hormone responses and root development. Overexpression of PtrXB38 in Populus led to significant increases in callusing and formation of both stem-born roots and base-born adventitious roots. Omics studies revealed that genes and proteins controlling auxin transport and signaling were involved in PtrXB38-mediated adventitious root formation. Protein–protein interaction assays indicated that PtrXB38 interacts with components of endosomal sorting complexes required for transport machinery, implying that PtrXB38-regulated root development may be mediated by regulating endocytosis pathway. Taken together, this work identified a crucial root development regulator and sheds light on the discovery of other plant developmental regulators through combining eQTL mapping and omics approaches.",

keywords = "Populus, PtrXB38, auxin signaling, developmental regulator, expression quantitative trait loci (eQTLs), stem-born root formation",

author = "Tao Yao and Jin Zhang and Yates, {Timothy B.} and Shrestha, {Him K.} and Engle, {Nancy L.} and Raphael Ployet and Cai John and Kai Feng and Bewg, {William Patrick} and Chen, {Margot S.S.} and Haiwei Lu and Harding, {Scott A.} and Zhenzhen Qiao and Jawdy, {Sara S.} and Mengjun Shu and Wenya Yuan and Khadijeh Mozaffari and Harman-Ware, {Anne E.} and Happs, {Renee M.} and York, {Larry M.} and Binder, {Brad M.} and Yuko Yoshinaga and Christopher Daum and Tschaplinski, {Timothy J.} and Abraham, {Paul E.} and Tsai, {Chung Jui} and Kerrie Barry and Anna Lipzen and Jeremy Schmutz and Tuskan, {Gerald A.} and Chen, {Jin Gui} and Wellington Muchero",

note = "Publisher Copyright: {\textcopyright} 2023 The Authors New Phytologist {\textcopyright} 2023 New Phytologist Foundation.",

year = "2023",

month = sep,

doi = "10.1111/nph.19126",

language = "English",

volume = "239",

pages = "2248--2264",

journal = "New Phytologist",

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Yao, T, Zhang, J, Yates, TB, Shrestha, HK, Engle, NL, Ployet, R, John, C, Feng, K, Bewg, WP, Chen, MSS, Lu, H, Harding, SA, Qiao, Z, Jawdy, SS, Shu, M, Yuan, W, Mozaffari, K, Harman-Ware, AE, Happs, RM, York, LM, Binder, BM, Yoshinaga, Y, Daum, C, Tschaplinski, TJ , Abraham, PE, Tsai, CJ, Barry, K, Lipzen, A, Schmutz, J, Tuskan, GA , Chen, JG & Muchero, W 2023, 'Expression quantitative trait loci mapping identified PtrXB38 as a key hub gene in adventitious root development in Populus', New Phytologist, vol. 239, no. 6, pp. 2248-2264. https://doi.org/10.1111/nph.19126

TY - JOUR

T1 - Expression quantitative trait loci mapping identified PtrXB38 as a key hub gene in adventitious root development in Populus

AU - Yao, Tao

AU - Zhang, Jin

AU - Yates, Timothy B.

AU - Shrestha, Him K.

AU - Engle, Nancy L.

AU - Ployet, Raphael

AU - John, Cai

AU - Feng, Kai

AU - Bewg, William Patrick

AU - Chen, Margot S.S.

AU - Lu, Haiwei

AU - Harding, Scott A.

AU - Qiao, Zhenzhen

AU - Jawdy, Sara S.

AU - Shu, Mengjun

AU - Yuan, Wenya

AU - Mozaffari, Khadijeh

AU - Harman-Ware, Anne E.

AU - Happs, Renee M.

AU - York, Larry M.

AU - Binder, Brad M.

AU - Yoshinaga, Yuko

AU - Daum, Christopher

AU - Tschaplinski, Timothy J.

AU - Abraham, Paul E.

AU - Tsai, Chung Jui

AU - Barry, Kerrie

AU - Lipzen, Anna

AU - Schmutz, Jeremy

AU - Tuskan, Gerald A.

AU - Chen, Jin Gui

AU - Muchero, Wellington

PY - 2023/9

Y1 - 2023/9

N2 - Plant establishment requires the formation and development of an extensive root system with architecture modulated by complex genetic networks. Here, we report the identification of the PtrXB38 gene as an expression quantitative trait loci (eQTL) hotspot, mapped using 390 leaf and 444 xylem Populus trichocarpa transcriptomes. Among predicted targets of this trans-eQTL were genes involved in plant hormone responses and root development. Overexpression of PtrXB38 in Populus led to significant increases in callusing and formation of both stem-born roots and base-born adventitious roots. Omics studies revealed that genes and proteins controlling auxin transport and signaling were involved in PtrXB38-mediated adventitious root formation. Protein–protein interaction assays indicated that PtrXB38 interacts with components of endosomal sorting complexes required for transport machinery, implying that PtrXB38-regulated root development may be mediated by regulating endocytosis pathway. Taken together, this work identified a crucial root development regulator and sheds light on the discovery of other plant developmental regulators through combining eQTL mapping and omics approaches.

AB - Plant establishment requires the formation and development of an extensive root system with architecture modulated by complex genetic networks. Here, we report the identification of the PtrXB38 gene as an expression quantitative trait loci (eQTL) hotspot, mapped using 390 leaf and 444 xylem Populus trichocarpa transcriptomes. Among predicted targets of this trans-eQTL were genes involved in plant hormone responses and root development. Overexpression of PtrXB38 in Populus led to significant increases in callusing and formation of both stem-born roots and base-born adventitious roots. Omics studies revealed that genes and proteins controlling auxin transport and signaling were involved in PtrXB38-mediated adventitious root formation. Protein–protein interaction assays indicated that PtrXB38 interacts with components of endosomal sorting complexes required for transport machinery, implying that PtrXB38-regulated root development may be mediated by regulating endocytosis pathway. Taken together, this work identified a crucial root development regulator and sheds light on the discovery of other plant developmental regulators through combining eQTL mapping and omics approaches.

KW - Populus

KW - PtrXB38

KW - auxin signaling

KW - developmental regulator

KW - expression quantitative trait loci (eQTLs)

KW - stem-born root formation

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U2 - 10.1111/nph.19126

DO - 10.1111/nph.19126

M3 - Article

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AN - SCOPUS:85165593971

SN - 0028-646X

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JO - New Phytologist

JF - New Phytologist

IS - 6

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Expression quantitative trait loci mapping identified PtrXB38 as a key hub gene in adventitious root development in Populus

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