Transcriptional and Morpho-Physiological Responses of <i>Marchantia polymorpha</i> upon Phosphate Starvation

Phosphate (Pi) is a pivotal nutrient that constraints plant development and productivity in natural ecosystems. Land colonization by plants, more than 470 million years ago, evolved adaptive mechanisms to conquer Pi-scarce environments. However, little is known about the molecular basis underlying s...

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Main Authors: Félix Rico-Reséndiz, Sergio Alan Cervantes-Pérez, Annie Espinal-Centeno, Melissa Dipp-Álvarez, Araceli Oropeza-Aburto, Enrique Hurtado-Bautista, Andrés Cruz-Hernández, John L. Bowman, Kimitsune Ishizaki, Mario A. Arteaga-Vázquez, Luis Herrera-Estrella, Alfredo Cruz-Ramírez
Format: Article
Language:English
Published: MDPI AG 2020-11-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/21/21/8354
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author Félix Rico-Reséndiz
Sergio Alan Cervantes-Pérez
Annie Espinal-Centeno
Melissa Dipp-Álvarez
Araceli Oropeza-Aburto
Enrique Hurtado-Bautista
Andrés Cruz-Hernández
John L. Bowman
Kimitsune Ishizaki
Mario A. Arteaga-Vázquez
Luis Herrera-Estrella
Alfredo Cruz-Ramírez
author_facet Félix Rico-Reséndiz
Sergio Alan Cervantes-Pérez
Annie Espinal-Centeno
Melissa Dipp-Álvarez
Araceli Oropeza-Aburto
Enrique Hurtado-Bautista
Andrés Cruz-Hernández
John L. Bowman
Kimitsune Ishizaki
Mario A. Arteaga-Vázquez
Luis Herrera-Estrella
Alfredo Cruz-Ramírez
author_sort Félix Rico-Reséndiz
collection DOAJ
description Phosphate (Pi) is a pivotal nutrient that constraints plant development and productivity in natural ecosystems. Land colonization by plants, more than 470 million years ago, evolved adaptive mechanisms to conquer Pi-scarce environments. However, little is known about the molecular basis underlying such adaptations at early branches of plant phylogeny. To shed light on how early divergent plants respond to Pi limitation, we analyzed the morpho-physiological and transcriptional dynamics of <i>Marchantia polymorpha</i> upon Pi starvation. Our phylogenomic analysis highlights some gene networks present since the Chlorophytes and others established in the Streptophytes (e.g., PHR1–SPX1 and STOP1–ALMT1, respectively). At the morpho-physiological level, the response is characterized by the induction of phosphatase activity, media acidification, accumulation of auronidins, reduction of internal Pi concentration, and developmental modifications of rhizoids. The transcriptional response involves the induction of Mp<i>PHR1</i>, Pi transporters, lipid turnover enzymes, and Mp<i>MYB14</i>, which is an essential transcription factor for auronidins biosynthesis. Mp<i>STOP2</i> up-regulation correlates with expression changes in genes related to organic acid biosynthesis and transport, suggesting a preference for citrate exudation. An analysis of MpPHR1 binding sequences (P1BS) shows an enrichment of this <i>cis</i> regulatory element in differentially expressed genes. Our study unravels the strategies, at diverse levels of organization, exerted by <i>M. polymorpha</i> to cope with low Pi availability.
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spelling doaj.art-6a5cc7daffe24d87a9974222ee7ec7d22023-11-20T20:07:13ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-11-012121835410.3390/ijms21218354Transcriptional and Morpho-Physiological Responses of <i>Marchantia polymorpha</i> upon Phosphate StarvationFélix Rico-Reséndiz0Sergio Alan Cervantes-Pérez1Annie Espinal-Centeno2Melissa Dipp-Álvarez3Araceli Oropeza-Aburto4Enrique Hurtado-Bautista5Andrés Cruz-Hernández6John L. Bowman7Kimitsune Ishizaki8Mario A. Arteaga-Vázquez9Luis Herrera-Estrella10Alfredo Cruz-Ramírez11Molecular and Developmental Complexity Group, Unidad de Genómica Avanzada, Centro de Investigación y Estudios Avanzados, Instituto Politécnico Nacional, Irapuato 36824, Guanajuato, MexicoPlant Physiology and Metabolic Engineering Group, Unidad de Genómica Avanzada, Centro de Investigación y Estudios Avanzados, Instituto Politécnico Nacional, Irapuato 36824, Guanajuato, MexicoMolecular and Developmental Complexity Group, Unidad de Genómica Avanzada, Centro de Investigación y Estudios Avanzados, Instituto Politécnico Nacional, Irapuato 36824, Guanajuato, MexicoMolecular and Developmental Complexity Group, Unidad de Genómica Avanzada, Centro de Investigación y Estudios Avanzados, Instituto Politécnico Nacional, Irapuato 36824, Guanajuato, MexicoPlant Physiology and Metabolic Engineering Group, Unidad de Genómica Avanzada, Centro de Investigación y Estudios Avanzados, Instituto Politécnico Nacional, Irapuato 36824, Guanajuato, MexicoMolecular Biology and Microbial Ecology, Unidad Irapuato, Centro de Investigación y Estudios Avanzados, Instituto Politécnico Nacional, Irapuato 36824, Guanajuato, MexicoEscuela de Agronomía, Universidad de La Salle Bajío, León 37160, Guanajuato, MexicoSchool of Biological Sciences, Monash University, Melbourne, Victoria 3800, AustraliaGraduate School of Science, Kobe University, Kobe 657-8501, JapanGroup of Epigenetics and Developmental Biology, Instituto de Biotecnología y Ecología Aplicada (INBIOTECA), Universidad Veracruzana, Xalapa 91640, MexicoPlant Physiology and Metabolic Engineering Group, Unidad de Genómica Avanzada, Centro de Investigación y Estudios Avanzados, Instituto Politécnico Nacional, Irapuato 36824, Guanajuato, MexicoMolecular and Developmental Complexity Group, Unidad de Genómica Avanzada, Centro de Investigación y Estudios Avanzados, Instituto Politécnico Nacional, Irapuato 36824, Guanajuato, MexicoPhosphate (Pi) is a pivotal nutrient that constraints plant development and productivity in natural ecosystems. Land colonization by plants, more than 470 million years ago, evolved adaptive mechanisms to conquer Pi-scarce environments. However, little is known about the molecular basis underlying such adaptations at early branches of plant phylogeny. To shed light on how early divergent plants respond to Pi limitation, we analyzed the morpho-physiological and transcriptional dynamics of <i>Marchantia polymorpha</i> upon Pi starvation. Our phylogenomic analysis highlights some gene networks present since the Chlorophytes and others established in the Streptophytes (e.g., PHR1–SPX1 and STOP1–ALMT1, respectively). At the morpho-physiological level, the response is characterized by the induction of phosphatase activity, media acidification, accumulation of auronidins, reduction of internal Pi concentration, and developmental modifications of rhizoids. The transcriptional response involves the induction of Mp<i>PHR1</i>, Pi transporters, lipid turnover enzymes, and Mp<i>MYB14</i>, which is an essential transcription factor for auronidins biosynthesis. Mp<i>STOP2</i> up-regulation correlates with expression changes in genes related to organic acid biosynthesis and transport, suggesting a preference for citrate exudation. An analysis of MpPHR1 binding sequences (P1BS) shows an enrichment of this <i>cis</i> regulatory element in differentially expressed genes. Our study unravels the strategies, at diverse levels of organization, exerted by <i>M. polymorpha</i> to cope with low Pi availability.https://www.mdpi.com/1422-0067/21/21/8354land plant evolution<i>Marchantia polymorpha</i>Pi starvation and RNA-seq
spellingShingle Félix Rico-Reséndiz
Sergio Alan Cervantes-Pérez
Annie Espinal-Centeno
Melissa Dipp-Álvarez
Araceli Oropeza-Aburto
Enrique Hurtado-Bautista
Andrés Cruz-Hernández
John L. Bowman
Kimitsune Ishizaki
Mario A. Arteaga-Vázquez
Luis Herrera-Estrella
Alfredo Cruz-Ramírez
Transcriptional and Morpho-Physiological Responses of <i>Marchantia polymorpha</i> upon Phosphate Starvation
International Journal of Molecular Sciences
land plant evolution
<i>Marchantia polymorpha</i>
Pi starvation and RNA-seq
title Transcriptional and Morpho-Physiological Responses of <i>Marchantia polymorpha</i> upon Phosphate Starvation
title_full Transcriptional and Morpho-Physiological Responses of <i>Marchantia polymorpha</i> upon Phosphate Starvation
title_fullStr Transcriptional and Morpho-Physiological Responses of <i>Marchantia polymorpha</i> upon Phosphate Starvation
title_full_unstemmed Transcriptional and Morpho-Physiological Responses of <i>Marchantia polymorpha</i> upon Phosphate Starvation
title_short Transcriptional and Morpho-Physiological Responses of <i>Marchantia polymorpha</i> upon Phosphate Starvation
title_sort transcriptional and morpho physiological responses of i marchantia polymorpha i upon phosphate starvation
topic land plant evolution
<i>Marchantia polymorpha</i>
Pi starvation and RNA-seq
url https://www.mdpi.com/1422-0067/21/21/8354
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