Divergence of expression pattern contributed to neofunctionalization of duplicated HD-Zip I transcription factor in barley

Shun Sakuma, Mohammad Pourkheirandish, Goetz Hensel, Jochen Kumlehn, Nils Stein, Akemi Tagiri, Naoki Yamaji, Jian Feng Ma, Hidenori Sassa, Takato Koba, Takao Komatsuda

Research output: Contribution to journalArticle

37 Citations (Scopus)

Abstract

Summary: Barley (Hordeum vulgare) spikes are developmentally switched from two-rowed to six-rowed by a single recessive gene, six-rowed spike 1 (vrs1), which encodes a homeodomain-leucine zipper I class transcription factor. Vrs1 is a paralog of HvHox2 and both were generated by duplication of an ancestral gene. HvHox2 is conserved among cereals, whereas Vrs1 acquired its current function during the evolution of barley. It was unclear whether divergence of expression pattern or protein function accounted for the functionalization of Vrs1. Here, we conducted a comparative analysis of protein functions and gene expression between HvHox2 and Vrs1 to clarify the functionalization mechanism. We revealed that the transcriptional activation activity of HvHOX2 and VRS1 was conserved. In situ hybridization analysis showed that HvHox2 is localized in vascular bundles in developing spikes, whereas Vrs1 is expressed exclusively in the pistil, lemma, palea and lodicule of lateral spikelets. The transcript abundance of Vrs1 was > 10-fold greater than that of HvHox2 during the pistil developmental stage, suggesting that the essential function of Vrs1 is to inhibit gynoecial development. We demonstrated the quantitative function of Vrs1 using RNAi transgenic plants and Vrs1 expression variants. Expression analysis of six-rowed spike mutants that are nonallelic to vrs1 showed that Vrs1 expression was up-regulated by Vrs4, whereas HvHox2 expression was not. These data demonstrate that the divergence of gene expression pattern contributed to the neofunctionalization of Vrs1.

Original languageEnglish
Pages (from-to)939-948
Number of pages10
JournalNew Phytologist
Volume197
Issue number3
DOIs
Publication statusPublished - Feb 2013

Fingerprint

Hordeum
Transcription Factors
inflorescences
transcription factors
barley
Recessive Genes
pistil
Gene Expression
Leucine Zippers
Gene Duplication
Genetically Modified Plants
RNA Interference
Transcriptional Activation
In Situ Hybridization
Blood Vessels
Proteins
leucine zipper
gene expression
recessive genes
vascular bundles

Keywords

  • Barley (Hordeum vulgare)
  • Gene duplication
  • HD-Zip I transcription factor
  • Neofunctionalization
  • Six-rowed spike

ASJC Scopus subject areas

  • Plant Science
  • Physiology

Cite this

Sakuma, S., Pourkheirandish, M., Hensel, G., Kumlehn, J., Stein, N., Tagiri, A., ... Komatsuda, T. (2013). Divergence of expression pattern contributed to neofunctionalization of duplicated HD-Zip I transcription factor in barley. New Phytologist, 197(3), 939-948. https://doi.org/10.1111/nph.12068

Divergence of expression pattern contributed to neofunctionalization of duplicated HD-Zip I transcription factor in barley. / Sakuma, Shun; Pourkheirandish, Mohammad; Hensel, Goetz; Kumlehn, Jochen; Stein, Nils; Tagiri, Akemi; Yamaji, Naoki; Ma, Jian Feng; Sassa, Hidenori; Koba, Takato; Komatsuda, Takao.

In: New Phytologist, Vol. 197, No. 3, 02.2013, p. 939-948.

Research output: Contribution to journalArticle

Sakuma, S, Pourkheirandish, M, Hensel, G, Kumlehn, J, Stein, N, Tagiri, A, Yamaji, N, Ma, JF, Sassa, H, Koba, T & Komatsuda, T 2013, 'Divergence of expression pattern contributed to neofunctionalization of duplicated HD-Zip I transcription factor in barley', New Phytologist, vol. 197, no. 3, pp. 939-948. https://doi.org/10.1111/nph.12068
Sakuma, Shun ; Pourkheirandish, Mohammad ; Hensel, Goetz ; Kumlehn, Jochen ; Stein, Nils ; Tagiri, Akemi ; Yamaji, Naoki ; Ma, Jian Feng ; Sassa, Hidenori ; Koba, Takato ; Komatsuda, Takao. / Divergence of expression pattern contributed to neofunctionalization of duplicated HD-Zip I transcription factor in barley. In: New Phytologist. 2013 ; Vol. 197, No. 3. pp. 939-948.
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abstract = "Summary: Barley (Hordeum vulgare) spikes are developmentally switched from two-rowed to six-rowed by a single recessive gene, six-rowed spike 1 (vrs1), which encodes a homeodomain-leucine zipper I class transcription factor. Vrs1 is a paralog of HvHox2 and both were generated by duplication of an ancestral gene. HvHox2 is conserved among cereals, whereas Vrs1 acquired its current function during the evolution of barley. It was unclear whether divergence of expression pattern or protein function accounted for the functionalization of Vrs1. Here, we conducted a comparative analysis of protein functions and gene expression between HvHox2 and Vrs1 to clarify the functionalization mechanism. We revealed that the transcriptional activation activity of HvHOX2 and VRS1 was conserved. In situ hybridization analysis showed that HvHox2 is localized in vascular bundles in developing spikes, whereas Vrs1 is expressed exclusively in the pistil, lemma, palea and lodicule of lateral spikelets. The transcript abundance of Vrs1 was > 10-fold greater than that of HvHox2 during the pistil developmental stage, suggesting that the essential function of Vrs1 is to inhibit gynoecial development. We demonstrated the quantitative function of Vrs1 using RNAi transgenic plants and Vrs1 expression variants. Expression analysis of six-rowed spike mutants that are nonallelic to vrs1 showed that Vrs1 expression was up-regulated by Vrs4, whereas HvHox2 expression was not. These data demonstrate that the divergence of gene expression pattern contributed to the neofunctionalization of Vrs1.",
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AU - Kumlehn, Jochen

AU - Stein, Nils

AU - Tagiri, Akemi

AU - Yamaji, Naoki

AU - Ma, Jian Feng

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N2 - Summary: Barley (Hordeum vulgare) spikes are developmentally switched from two-rowed to six-rowed by a single recessive gene, six-rowed spike 1 (vrs1), which encodes a homeodomain-leucine zipper I class transcription factor. Vrs1 is a paralog of HvHox2 and both were generated by duplication of an ancestral gene. HvHox2 is conserved among cereals, whereas Vrs1 acquired its current function during the evolution of barley. It was unclear whether divergence of expression pattern or protein function accounted for the functionalization of Vrs1. Here, we conducted a comparative analysis of protein functions and gene expression between HvHox2 and Vrs1 to clarify the functionalization mechanism. We revealed that the transcriptional activation activity of HvHOX2 and VRS1 was conserved. In situ hybridization analysis showed that HvHox2 is localized in vascular bundles in developing spikes, whereas Vrs1 is expressed exclusively in the pistil, lemma, palea and lodicule of lateral spikelets. The transcript abundance of Vrs1 was > 10-fold greater than that of HvHox2 during the pistil developmental stage, suggesting that the essential function of Vrs1 is to inhibit gynoecial development. We demonstrated the quantitative function of Vrs1 using RNAi transgenic plants and Vrs1 expression variants. Expression analysis of six-rowed spike mutants that are nonallelic to vrs1 showed that Vrs1 expression was up-regulated by Vrs4, whereas HvHox2 expression was not. These data demonstrate that the divergence of gene expression pattern contributed to the neofunctionalization of Vrs1.

AB - Summary: Barley (Hordeum vulgare) spikes are developmentally switched from two-rowed to six-rowed by a single recessive gene, six-rowed spike 1 (vrs1), which encodes a homeodomain-leucine zipper I class transcription factor. Vrs1 is a paralog of HvHox2 and both were generated by duplication of an ancestral gene. HvHox2 is conserved among cereals, whereas Vrs1 acquired its current function during the evolution of barley. It was unclear whether divergence of expression pattern or protein function accounted for the functionalization of Vrs1. Here, we conducted a comparative analysis of protein functions and gene expression between HvHox2 and Vrs1 to clarify the functionalization mechanism. We revealed that the transcriptional activation activity of HvHOX2 and VRS1 was conserved. In situ hybridization analysis showed that HvHox2 is localized in vascular bundles in developing spikes, whereas Vrs1 is expressed exclusively in the pistil, lemma, palea and lodicule of lateral spikelets. The transcript abundance of Vrs1 was > 10-fold greater than that of HvHox2 during the pistil developmental stage, suggesting that the essential function of Vrs1 is to inhibit gynoecial development. We demonstrated the quantitative function of Vrs1 using RNAi transgenic plants and Vrs1 expression variants. Expression analysis of six-rowed spike mutants that are nonallelic to vrs1 showed that Vrs1 expression was up-regulated by Vrs4, whereas HvHox2 expression was not. These data demonstrate that the divergence of gene expression pattern contributed to the neofunctionalization of Vrs1.

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