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Gene dosage effects and signatures of purifying selection in lateral organ boundaries domain (LBD) genes LBD1 and LBD18

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Abstract

Wood formation is an economically and environmentally important process and has played a significant role in the evolution of terrestrial plants. Despite its significance, the molecular underpinnings of the process are still poorly understood. We have previously shown that four lateral organ boundaries (LBD) transcription factors have important roles in the regulation of secondary (woody) growth with two (LBD1 and LBD4) involved in secondary phloem and ray cell development and two (LBD15 and LBD18) in secondary xylem formation. We studied gene copy number and variation in DNA and amino acid sequences of the four LBDs in a wide range of woody and herbaceous plant taxa with fully sequenced and annotated genomes. LBD1 showed the highest gene copy number across species, and gene copy number was strongly and significantly correlated with tangential ray width. The climbing vines, cucumber and grape, with wide multiseriate rays (>10 cells wide) showed the highest gene copy number. Because the growth habit of woody lianas like grape requires significant twisting and bending, it was suggested that the unlignified ray parenchyma cells likely facilitate stem flexibility and maintenance of xylem conductivity. We further demonstrate conservation of amino acids in LBD18 protein sequences specific to woody taxa downstream of the LBD domain. Neutrality tests showed evidence for strong purifying selection on these regions across various orders, indicating important functional roles in woody taxa. Additionally, structural modeling demonstrates that these regions have a significant impact on tertiary protein structure and thus are likely of significant functional importance.

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Acknowledgments

Funding for the project was provided by the USDA-NIFA grant (2012-67013-19389) to VB, YY and OG. We would also like to thank the Biochemistry and Molecular Biology program at Michigan Technological University (MTU) which supported the research for one semester. Additional support was made available by MTU’s Ecosystem Science and Biotech Research Center. We would like to thank for the very constructive comments from two anonymous reviewers.

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Authors and Affiliations

  1. School of Forest Resources and Environmental Science, Michigan Technological University, 1400 Townsend Drive, Houghton, MI, 49931, USA

    Roba Bdeir, Victor Busov, Yordan Yordanov & Oliver Gailing

  2. Department of Biological Sciences, Eastern Illinois University, Charleston, IL, 61920, USA

    Yordan Yordanov

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  1. Roba Bdeir
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  2. Victor Busov
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  3. Yordan Yordanov
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Correspondence to Oliver Gailing.

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This study was funded by the USDA-NIFA grant (grant number 2012-67013-19389).

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Handling editor: Günter Theißen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

606_2015_1272_MOESM1_ESM.pdf

Neighbor-Joining tree based on complete protein sequences of all LBD genes from Arabidopsis thaliana and Brassica rapa. LBD homologs and gene copy numbers for each species are determined by the position in the phylogenetic tree relative to Arabidopsis thaliana LBD genes (PDF 35 kb)

606_2015_1272_MOESM2_ESM.pdf

Neighbor-Joining tree based on complete protein sequences of LBD1 genes. Bootstrap values above 50 and genes from woody species are highlighted in yellow (PDF 394 kb)

606_2015_1272_MOESM3_ESM.pdf

Neighbor-Joining tree based on complete protein sequences of LBD4 genes. Bootstrap values above 50 and genes from woody species are highlighted in yellow (PDF 277 kb)

606_2015_1272_MOESM4_ESM.pdf

Neighbor-Joining tree based on complete protein sequences of LBD15 genes. Bootstrap values above 50 and genes from woody species are highlighted in yellow (PDF 288 kb)

606_2015_1272_MOESM5_ESM.pdf

Neighbor-Joining tree based on complete protein sequences of LBD18 genes. Bootstrap values above 50 and genes from woody species are highlighted in yellow (PDF 47 kb)

606_2015_1272_MOESM6_ESM.pdf

Neighbor-Joining tree based on complete DNA coding sequences of LBD18 genes. Bootstrap values above 50 and genes from woody species are highlighted in yellow (PDF 47 kb)

Information on Electronic Supplementary Material

Information on Electronic Supplementary Material

Online Resource 1. Neighbor-Joining tree based on complete protein sequences of all LBD genes from Arabidopsis thaliana and Brassica rapa. LBD homologs and gene copy numbers for each species are determined by the position in the phylogenetic tree relative to Arabidopsis thaliana LBD genes.

Online Resource 2. Neighbor-Joining tree based on complete protein sequences of LBD1 genes. Bootstrap values above 50 and genes from woody species are highlighted in yellow.

Online Resource 3. Neighbor-Joining tree based on complete protein sequences of LBD4 genes. Bootstrap values above 50 and genes from woody species are highlighted in yellow.

Online Resource 4. Neighbor-Joining tree based on complete protein sequences of LBD15 genes. Bootstrap values above 50 and genes from woody species are highlighted in yellow.

Online Resource 5. Neighbor-Joining tree based on complete protein sequences of LBD18 genes. Bootstrap values above 50 and genes from woody species are highlighted in yellow.

Online Resource 6. Neighbor-Joining tree based on complete DNA coding sequences of LBD18 genes. Bootstrap values above 50 and genes from woody species are highlighted in yellow.

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Bdeir, R., Busov, V., Yordanov, Y. et al. Gene dosage effects and signatures of purifying selection in lateral organ boundaries domain (LBD) genes LBD1 and LBD18. Plant Syst Evol 302, 433–445 (2016). https://doi.org/10.1007/s00606-015-1272-4

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