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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2020-11-01
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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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issn | 1661-6596 1422-0067 |
language | English |
last_indexed | 2024-03-10T15:02:07Z |
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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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