Evidence for phloem loading via the abaxial bundle sheath cells in maize leaves
Leaves are asymmetric, with different functions for adaxial and abaxial tissue. The bundle sheath (BS) of C3 barley (Hordeum vulgare) is dorsoventrally differentiated into three types of cells: adaxial structural, lateral S-type, and abaxial L-type BS cells. Based on plasmodesmatal connections betwe...
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| Published in | The Plant cell Vol. 33; no. 3; pp. 531 - 547 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
05.05.2021
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| Online Access | Get full text |
| ISSN | 1532-298X 1532-298X |
| DOI | 10.1093/plcell/koaa055 |
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| Abstract | Leaves are asymmetric, with different functions for adaxial and abaxial tissue. The bundle sheath (BS) of C3 barley (Hordeum vulgare) is dorsoventrally differentiated into three types of cells: adaxial structural, lateral S-type, and abaxial L-type BS cells. Based on plasmodesmatal connections between S-type cells and mestome sheath (parenchymatous cell layer below bundle sheath), S-type cells likely transfer assimilates toward the phloem. Here, we used single-cell RNA sequencing to investigate BS differentiation in C4 maize (Zea mays L.) plants. Abaxial BS (abBS) cells of rank-2 intermediate veins specifically expressed three SWEET sucrose uniporters (SWEET13a, b, and c) and UmamiT amino acid efflux transporters. SWEET13a, b, c mRNAs were also detected in the phloem parenchyma (PP). We show that maize has acquired a mechanism for phloem loading in which abBS cells provide the main route for apoplasmic sucrose transfer toward the phloem. This putative route predominates in veins responsible for phloem loading (rank-2 intermediate), whereas rank-1 intermediate and major veins export sucrose from the PP adjacent to the sieve element companion cell complex, as in Arabidopsis thaliana. We surmise that abBS identity is subject to dorsoventral patterning and has components of PP identity. These observations provide insights into the unique transport-specific properties of abBS cells and support a modification to the canonical phloem loading pathway in maize. |
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| AbstractList | Leaves are asymmetric, with different functions for adaxial and abaxial tissue. The bundle sheath (BS) of C3 barley (Hordeum vulgare) is dorsoventrally differentiated into three types of cells: adaxial structural, lateral S-type, and abaxial L-type BS cells. Based on plasmodesmatal connections between S-type cells and mestome sheath (parenchymatous cell layer below bundle sheath), S-type cells likely transfer assimilates toward the phloem. Here, we used single-cell RNA sequencing to investigate BS differentiation in C4 maize (Zea mays L.) plants. Abaxial BS (abBS) cells of rank-2 intermediate veins specifically expressed three SWEET sucrose uniporters (SWEET13a, b, and c) and UmamiT amino acid efflux transporters. SWEET13a, b, c mRNAs were also detected in the phloem parenchyma (PP). We show that maize has acquired a mechanism for phloem loading in which abBS cells provide the main route for apoplasmic sucrose transfer toward the phloem. This putative route predominates in veins responsible for phloem loading (rank-2 intermediate), whereas rank-1 intermediate and major veins export sucrose from the PP adjacent to the sieve element companion cell complex, as in Arabidopsis thaliana. We surmise that abBS identity is subject to dorsoventral patterning and has components of PP identity. These observations provide insights into the unique transport-specific properties of abBS cells and support a modification to the canonical phloem loading pathway in maize.Leaves are asymmetric, with different functions for adaxial and abaxial tissue. The bundle sheath (BS) of C3 barley (Hordeum vulgare) is dorsoventrally differentiated into three types of cells: adaxial structural, lateral S-type, and abaxial L-type BS cells. Based on plasmodesmatal connections between S-type cells and mestome sheath (parenchymatous cell layer below bundle sheath), S-type cells likely transfer assimilates toward the phloem. Here, we used single-cell RNA sequencing to investigate BS differentiation in C4 maize (Zea mays L.) plants. Abaxial BS (abBS) cells of rank-2 intermediate veins specifically expressed three SWEET sucrose uniporters (SWEET13a, b, and c) and UmamiT amino acid efflux transporters. SWEET13a, b, c mRNAs were also detected in the phloem parenchyma (PP). We show that maize has acquired a mechanism for phloem loading in which abBS cells provide the main route for apoplasmic sucrose transfer toward the phloem. This putative route predominates in veins responsible for phloem loading (rank-2 intermediate), whereas rank-1 intermediate and major veins export sucrose from the PP adjacent to the sieve element companion cell complex, as in Arabidopsis thaliana. We surmise that abBS identity is subject to dorsoventral patterning and has components of PP identity. These observations provide insights into the unique transport-specific properties of abBS cells and support a modification to the canonical phloem loading pathway in maize. Leaves are asymmetric, with different functions for adaxial and abaxial tissue. The bundle sheath (BS) of C3 barley (Hordeum vulgare) is dorsoventrally differentiated into three types of cells: adaxial structural, lateral S-type, and abaxial L-type BS cells. Based on plasmodesmatal connections between S-type cells and mestome sheath (parenchymatous cell layer below bundle sheath), S-type cells likely transfer assimilates toward the phloem. Here, we used single-cell RNA sequencing to investigate BS differentiation in C4 maize (Zea mays L.) plants. Abaxial BS (abBS) cells of rank-2 intermediate veins specifically expressed three SWEET sucrose uniporters (SWEET13a, b, and c) and UmamiT amino acid efflux transporters. SWEET13a, b, c mRNAs were also detected in the phloem parenchyma (PP). We show that maize has acquired a mechanism for phloem loading in which abBS cells provide the main route for apoplasmic sucrose transfer toward the phloem. This putative route predominates in veins responsible for phloem loading (rank-2 intermediate), whereas rank-1 intermediate and major veins export sucrose from the PP adjacent to the sieve element companion cell complex, as in Arabidopsis thaliana. We surmise that abBS identity is subject to dorsoventral patterning and has components of PP identity. These observations provide insights into the unique transport-specific properties of abBS cells and support a modification to the canonical phloem loading pathway in maize. |
| Author | Kruse, Colin P S Lautwein, Tobias Frommer, Wolf B Köhrer, Karl Kim, Ji-Yun Bezrutczyk, Margaret Hartwig, Thomas Zöllner, Nora R |
| Author_xml | – sequence: 1 givenname: Margaret orcidid: 0000-0002-8009-3635 surname: Bezrutczyk fullname: Bezrutczyk, Margaret organization: Institute for Molecular Physiology, Heinrich-Heine-University Düsseldorf, Düsseldorf 40225, Germany – sequence: 2 givenname: Nora R orcidid: 0000-0002-0961-5680 surname: Zöllner fullname: Zöllner, Nora R organization: Institute for Molecular Physiology, Heinrich-Heine-University Düsseldorf, Düsseldorf 40225, Germany – sequence: 3 givenname: Colin P S orcidid: 0000-0001-7070-8889 surname: Kruse fullname: Kruse, Colin P S organization: Los Alamos National Laboratory, Los Alamos, New Mexico 87545, USA – sequence: 4 givenname: Thomas orcidid: 0000-0002-2707-2771 surname: Hartwig fullname: Hartwig, Thomas organization: Institute for Molecular Physiology, Heinrich-Heine-University Düsseldorf, Düsseldorf 40225, Germany – sequence: 5 givenname: Tobias orcidid: 0000-0002-3872-3613 surname: Lautwein fullname: Lautwein, Tobias organization: Biological and Medical Research Center (BMFZ), Genomics and Transcriptomics Laboratory (GTL), Medical Faculty, Heinrich Heine University Düsseldorf, Düsseldorf 40225, Germany – sequence: 6 givenname: Karl orcidid: 0000-0003-3644-2022 surname: Köhrer fullname: Köhrer, Karl organization: Biological and Medical Research Center (BMFZ), Genomics and Transcriptomics Laboratory (GTL), Medical Faculty, Heinrich Heine University Düsseldorf, Düsseldorf 40225, Germany – sequence: 7 givenname: Wolf B orcidid: 0000-0001-6465-0115 surname: Frommer fullname: Frommer, Wolf B organization: Institute for Molecular Physiology, Heinrich-Heine-University Düsseldorf, Düsseldorf 40225, Germany, Institute of Transformative Bio-Molecules (WPI-ITbM), Nagoya University, Chikusa, Nagoya 464-8601, Japan – sequence: 8 givenname: Ji-Yun orcidid: 0000-0003-2776-5970 surname: Kim fullname: Kim, Ji-Yun organization: Institute for Molecular Physiology, Heinrich-Heine-University Düsseldorf, Düsseldorf 40225, Germany |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33793854$$D View this record in MEDLINE/PubMed |
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| Copyright | The Author(s) 2021. Published by Oxford University Press on behalf of American Society of Plant Biologists. |
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| Title | Evidence for phloem loading via the abaxial bundle sheath cells in maize leaves |
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