Cytokinin signaling regulates cambial development in poplar

Kaisa Nieminen, Juha Immanen, Marjukka Laxell, Leila Kauppinen, Petr Tarkowski, Karel Dolezal, Sari Tähtiharju, Annakaisa Elo, Melanie Decourteix, Karin Ljung, Rishikesh Bhalerao, Kaija Keinonen, Victor A Albert, Yrjö Helariutta

Research output: Contribution to journalArticleScientificpeer-review

Abstract

Although a substantial proportion of plant biomass originates from the activity of vascular cambium, the molecular basis of radial plant growth is still largely unknown. To address whether cytokinins are required for cambial activity, we studied cytokinin signaling across the cambial zones of 2 tree species, poplar (Populus trichocarpa) and birch (Betula pendula). We observed an expression peak for genes encoding cytokinin receptors in the dividing cambial cells. We reduced cytokinin levels endogenously by engineering transgenic poplar trees (P. tremula x tremuloides) to express a cytokinin catabolic gene, Arabidopsis CYTOKININ OXIDASE 2, under the promoter of a birch CYTOKININ RECEPTOR 1 gene. Transgenic trees showed reduced concentration of a biologically active cytokinin, correlating with impaired cytokinin responsiveness. In these trees, both apical and radial growth was compromised. However, radial growth was more affected, as illustrated by a thinner stem diameter than in WT at same height. To dissect radial from apical growth inhibition, we performed a reciprocal grafting experiment. WT scion outgrew the diameter of transgenic stock, implicating cytokinin activity as a direct determinant of radial growth. The reduced radial growth correlated with a reduced number of cambial cell layers. Moreover, expression of a cytokinin primary response gene was dramatically reduced in the thin-stemmed transgenic trees. Thus, a reduced level of cytokinin signaling is the primary basis for the impaired cambial growth observed. Together, our results show that cytokinins are major hormonal regulators required for cambial development.
Original languageEnglish
JournalProceedings of the National Academy of Sciences of the United States of America
Volume105
Issue number50
Pages (from-to)20032-20037
Number of pages6
ISSN0027-8424
DOIs
Publication statusPublished - 2008
MoE publication typeA1 Journal article-refereed

Cite this

Nieminen, Kaisa ; Immanen, Juha ; Laxell, Marjukka ; Kauppinen, Leila ; Tarkowski, Petr ; Dolezal, Karel ; Tähtiharju, Sari ; Elo, Annakaisa ; Decourteix, Melanie ; Ljung, Karin ; Bhalerao, Rishikesh ; Keinonen, Kaija ; Albert, Victor A ; Helariutta, Yrjö. / Cytokinin signaling regulates cambial development in poplar. In: Proceedings of the National Academy of Sciences of the United States of America. 2008 ; Vol. 105, No. 50. pp. 20032-20037.
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title = "Cytokinin signaling regulates cambial development in poplar",
abstract = "Although a substantial proportion of plant biomass originates from the activity of vascular cambium, the molecular basis of radial plant growth is still largely unknown. To address whether cytokinins are required for cambial activity, we studied cytokinin signaling across the cambial zones of 2 tree species, poplar (Populus trichocarpa) and birch (Betula pendula). We observed an expression peak for genes encoding cytokinin receptors in the dividing cambial cells. We reduced cytokinin levels endogenously by engineering transgenic poplar trees (P. tremula x tremuloides) to express a cytokinin catabolic gene, Arabidopsis CYTOKININ OXIDASE 2, under the promoter of a birch CYTOKININ RECEPTOR 1 gene. Transgenic trees showed reduced concentration of a biologically active cytokinin, correlating with impaired cytokinin responsiveness. In these trees, both apical and radial growth was compromised. However, radial growth was more affected, as illustrated by a thinner stem diameter than in WT at same height. To dissect radial from apical growth inhibition, we performed a reciprocal grafting experiment. WT scion outgrew the diameter of transgenic stock, implicating cytokinin activity as a direct determinant of radial growth. The reduced radial growth correlated with a reduced number of cambial cell layers. Moreover, expression of a cytokinin primary response gene was dramatically reduced in the thin-stemmed transgenic trees. Thus, a reduced level of cytokinin signaling is the primary basis for the impaired cambial growth observed. Together, our results show that cytokinins are major hormonal regulators required for cambial development.",
author = "Kaisa Nieminen and Juha Immanen and Marjukka Laxell and Leila Kauppinen and Petr Tarkowski and Karel Dolezal and Sari T{\"a}htiharju and Annakaisa Elo and Melanie Decourteix and Karin Ljung and Rishikesh Bhalerao and Kaija Keinonen and Albert, {Victor A} and Yrj{\"o} Helariutta",
year = "2008",
doi = "10.1073/pnas.0805617106",
language = "English",
volume = "105",
pages = "20032--20037",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
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Nieminen, K, Immanen, J, Laxell, M, Kauppinen, L, Tarkowski, P, Dolezal, K, Tähtiharju, S, Elo, A, Decourteix, M, Ljung, K, Bhalerao, R, Keinonen, K, Albert, VA & Helariutta, Y 2008, 'Cytokinin signaling regulates cambial development in poplar' Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 50, pp. 20032-20037. https://doi.org/10.1073/pnas.0805617106

Cytokinin signaling regulates cambial development in poplar. / Nieminen, Kaisa; Immanen, Juha; Laxell, Marjukka; Kauppinen, Leila; Tarkowski, Petr; Dolezal, Karel; Tähtiharju, Sari; Elo, Annakaisa; Decourteix, Melanie; Ljung, Karin; Bhalerao, Rishikesh; Keinonen, Kaija; Albert, Victor A; Helariutta, Yrjö.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 105, No. 50, 2008, p. 20032-20037.

Research output: Contribution to journalArticleScientificpeer-review

TY - JOUR

T1 - Cytokinin signaling regulates cambial development in poplar

AU - Nieminen, Kaisa

AU - Immanen, Juha

AU - Laxell, Marjukka

AU - Kauppinen, Leila

AU - Tarkowski, Petr

AU - Dolezal, Karel

AU - Tähtiharju, Sari

AU - Elo, Annakaisa

AU - Decourteix, Melanie

AU - Ljung, Karin

AU - Bhalerao, Rishikesh

AU - Keinonen, Kaija

AU - Albert, Victor A

AU - Helariutta, Yrjö

PY - 2008

Y1 - 2008

N2 - Although a substantial proportion of plant biomass originates from the activity of vascular cambium, the molecular basis of radial plant growth is still largely unknown. To address whether cytokinins are required for cambial activity, we studied cytokinin signaling across the cambial zones of 2 tree species, poplar (Populus trichocarpa) and birch (Betula pendula). We observed an expression peak for genes encoding cytokinin receptors in the dividing cambial cells. We reduced cytokinin levels endogenously by engineering transgenic poplar trees (P. tremula x tremuloides) to express a cytokinin catabolic gene, Arabidopsis CYTOKININ OXIDASE 2, under the promoter of a birch CYTOKININ RECEPTOR 1 gene. Transgenic trees showed reduced concentration of a biologically active cytokinin, correlating with impaired cytokinin responsiveness. In these trees, both apical and radial growth was compromised. However, radial growth was more affected, as illustrated by a thinner stem diameter than in WT at same height. To dissect radial from apical growth inhibition, we performed a reciprocal grafting experiment. WT scion outgrew the diameter of transgenic stock, implicating cytokinin activity as a direct determinant of radial growth. The reduced radial growth correlated with a reduced number of cambial cell layers. Moreover, expression of a cytokinin primary response gene was dramatically reduced in the thin-stemmed transgenic trees. Thus, a reduced level of cytokinin signaling is the primary basis for the impaired cambial growth observed. Together, our results show that cytokinins are major hormonal regulators required for cambial development.

AB - Although a substantial proportion of plant biomass originates from the activity of vascular cambium, the molecular basis of radial plant growth is still largely unknown. To address whether cytokinins are required for cambial activity, we studied cytokinin signaling across the cambial zones of 2 tree species, poplar (Populus trichocarpa) and birch (Betula pendula). We observed an expression peak for genes encoding cytokinin receptors in the dividing cambial cells. We reduced cytokinin levels endogenously by engineering transgenic poplar trees (P. tremula x tremuloides) to express a cytokinin catabolic gene, Arabidopsis CYTOKININ OXIDASE 2, under the promoter of a birch CYTOKININ RECEPTOR 1 gene. Transgenic trees showed reduced concentration of a biologically active cytokinin, correlating with impaired cytokinin responsiveness. In these trees, both apical and radial growth was compromised. However, radial growth was more affected, as illustrated by a thinner stem diameter than in WT at same height. To dissect radial from apical growth inhibition, we performed a reciprocal grafting experiment. WT scion outgrew the diameter of transgenic stock, implicating cytokinin activity as a direct determinant of radial growth. The reduced radial growth correlated with a reduced number of cambial cell layers. Moreover, expression of a cytokinin primary response gene was dramatically reduced in the thin-stemmed transgenic trees. Thus, a reduced level of cytokinin signaling is the primary basis for the impaired cambial growth observed. Together, our results show that cytokinins are major hormonal regulators required for cambial development.

U2 - 10.1073/pnas.0805617106

DO - 10.1073/pnas.0805617106

M3 - Article

VL - 105

SP - 20032

EP - 20037

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 50

ER -