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Nuclear, chloroplast, and mitochondrial transcript abundance along a maize leaf developmental gradient

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Abstract

In maize, the chloroplast chromosome encodes 104 genes whose roles are primarily in photosynthesis and gene expression. The 2,000–3,000 nuclear gene products that localize to plastids are required both to encode and regulate plastid gene expression as well as to underpin each aspect of plastid physiology and development. We used a new “three-genome” maize biogenesis cDNA microarray to track abundance changes in nuclear, chloroplast and mitochondrial transcripts in stage 2 semi-emerged leaf blades of one month-old maize plants. We report the detection and quantification of 433 nuclear, 62 chloroplast, and 27 mitochondrial transcripts, with the majority of the nuclear transcripts predicted or known to encode plastid proteins. The data were analyzed as ratios of expression of individual transcripts in the green tip (mature chloroplasts) versus the yellow base of the leaf (etioplasts). According to the microarray data at least 51 plastid genes and 121 nuclear genes are expressed at least two-fold higher in the tip of the leaf. Almost all (25) mitochondrial and 177 nuclear transcripts were expressed at least 2–fold higher in the leaf base. Independent quantification of a subset of each transcript population by RNA gel blot analysis and/or quantitative real time RT-PCR concurred with the transcript ratios determined by the array. Ontological distribution of the transcripts suggests that photosynthesis-related RNAs were most highly abundant in the leaf tip and that energy use genes were most highly expressed in the base. Transcripts whose products are used in plastid translation constituted the largest single ontological group with relatively equal numbers of genes in the three expression categories, defined as higher in tip, higher in base, or equally expressed in tip and base.

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Abbreviations

CTP:

plastid targeted proteins

Q-2RT-PCR:

quantitative, real-time, reverse transcriptase polymerase chain reaction

EST:

expressed sequence tag

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Acknowledgements

The authors wish to thank Qi Sun (Cornell University) for initial bioinformatic screening of microarray components and Timothy Setter of Cornell University for the Unigene I library. Members of Tom Brutnell’s lab at BTI helped with sequencing and design of the array. Arnaud Germain (BTI) provided technical assistance with gel blot analysis. Helpful discussion and comments were provided by Thomas J. Bollenbach, members of the Stern lab (BTI), and the Three Stooges lab (MTSU). Work in the Stern laboratory was supported by NSF award DBI-0211935, work at MTSU was supported by an internal research enhancement program.

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  1. Elizabeth M. Takacs

    Present address: Department of Plant Biology, Cornell University, Ithaca, NY, 14853, USA

Authors and Affiliations

  1. Department of Biology, Middle Tennessee State University, P.O. Box 60, Murfreesboro, TN, 37132, USA

    A. Bruce Cahoon & Richard M. Sharpe

  2. Boyce Thompson Institute for Plant Research, Tower Rd, Ithaca, NY, 14853, USA

    Elizabeth M. Takacs & David B. Stern

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Correspondence to A. Bruce Cahoon.

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Table S1

Primers Used for Quantitative Real Time RT-PCR Analysis. Sets were designed based on GenBank accessions. The members of each set have a similar annealing temperature and are predicted to resist forming secondary structure at or above these temperatures. Amplicons are 75–150 bases in size (DOC 22 kb)

Table S2

Microarray elements. A complete list of the elements included on the maize three genome microarray developed at Boyce Thompson Institute. Listed are nuclear, chloroplast, and mitochondrial genes as well as positive control spots, negative control spots, and blanks (XLS 469 kb)

Table S3

Chloroplast transcripts. A list of the protein-coding chloroplast transcripts detected by the microarray experiments which passed the data quality screens described in Materials and Methods. The genes are arranged by their Tip:Base ratio from the smallest ratio to the largest (XLS 36 kb)

Table S4

Mitochondrial transcripts. A list of the protein-coding mitochondrial transcripts detected by the microarray experiments which passed the data quality screens described in Materials and Methods. The genes are arranged by their Tip:Base ratio from the smallest ratio to the largest (XLS 21 kb)

Table S5

Nuclear gene transcripts, higher in base. A list of the nuclear transcripts with a Tip:Base ratio which suggested they were most abundant in the base of the leaf. The genes are arranged by their Tip:Base ratio from smallest (expressed most extremely in the base) to ratios close to the cutoff of 0.5 (0.5 represents a two-fold difference in transcript abundance in the base and the tip) (XLS 70 kb)

Table S6

Nuclear gene transcripts, no change. A list of the nuclear transcripts with a Tip:Base ratio which suggested there was less than two-fold abundance difference between the base and the tip. The genes are arranged by their Tip:Base ratios from just above two-fold higher in the base (0.5) to just below two fold higher in the tip (2.0) (XLS 54 kb)

Table S7

Nuclear gene transcripts, higher in tip. A list of the nuclear transcripts with a Tip:Base ratio which suggested they were most abundant in the tip of the leaf. The genes are arranged by their Tip:Base ratios from smallest (just above a two-fold difference in expression) to ratios indicating an extremely high transcript abundance in the tip versus the base (XLS 50 kb)

Table S8

MapMan Asignments. Nuclear genes with Arabidopsis homologs recognized by the MapMan program are listed. Bin designations are listed for each maize gene along with their array-derived expression ratios and the corresponding Arabidopsis locus numbers (XLS 66 kb)

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Cahoon, A.B., Takacs, E.M., Sharpe, R.M. et al. Nuclear, chloroplast, and mitochondrial transcript abundance along a maize leaf developmental gradient. Plant Mol Biol 66, 33–46 (2008). https://doi.org/10.1007/s11103-007-9250-z

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