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Endopolyploidy changes with age-related polyethism in the honey bee, Apis mellifera.

Rangel J, Strauss K, Seedorf K, Hjelmen CE, Johnston JS - PLoS ONE (2015)

Bottom Line: We found a nonsignificant increase in ploidy levels with age (P < 0.1) in the most highly endopolyploid secretory cells, the Malpighian tubules.Endopolyploidy decreased the least amount (nonsignificant) in neural (brain) cells and the stinger (P < 0.1).There was a significant reduction of endopolyploidy with age in leg (P < 0.05) and thoracic (P < 0.001) muscles.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, Texas A&M University, College Station, Texas 77843, United States of America.

ABSTRACT
Honey bees (Apis mellifera) exhibit age polyethism, whereby female workers assume increasingly complex colony tasks as they age. While changes in DNA methylation accompany age polyethism, other DNA modifications accompanying age polyethism are less known. Changes in endopolyploidy (DNA amplification in the absence of cell division) with increased larval age are typical in many insect cells and are essential in adults for creating larger cells, more copies of essential loci, or greater storage capacity in secretory cells. However, changes in endopolyploidy with increased adult worker age and polyethism are unstudied. In this study, we examined endopolyploidy in honey bee workers ranging in age from newly emerged up to 55 days old. We found a nonsignificant increase in ploidy levels with age (P < 0.1) in the most highly endopolyploid secretory cells, the Malpighian tubules. All other cell types decreased ploidy levels with age. Endopolyploidy decreased the least amount (nonsignificant) in neural (brain) cells and the stinger (P < 0.1). There was a significant reduction of endopolyploidy with age in leg (P < 0.05) and thoracic (P < 0.001) muscles. Ploidy in thoracic muscle dropped from an average of 0.5 rounds of replication in newly emerged workers to essentially no rounds of replication (0.125) in the oldest workers. Ploidy reduction in flight muscle cells is likely due to the production of G1 (2C) nuclei by amitotic division in the multinucleate striated flight muscles that are essential to foragers, the oldest workers. We suggest that ploidy is constrained by the shape, size and makeup of the multinucleate striated muscle cells. Furthermore, the presence of multiple 2C nuclei might be optimal for cell function, while higher ploidy levels might be a dead-end strategy of some aging adult tissues, likely used to increase cell size and storage capacity in secretory cells.

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Histograms showing fluorescence peaks centered at mean fluorescence channels 25, 50, 100, 200, and 400 produced by 2N, 4N, 8N, 16N and 32N nuclei isolated from flight muscle of (A) a 3-day-old and (B) a 27-day-old worker bee.The count of nuclei under each peak and the average ploidy level are given immediately below each histogram. The reported significant reduction of ploidy with age (P < 0.01) is reflected in the reduced 8N peak and 16N peak in the older bee.
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pone.0122208.g002: Histograms showing fluorescence peaks centered at mean fluorescence channels 25, 50, 100, 200, and 400 produced by 2N, 4N, 8N, 16N and 32N nuclei isolated from flight muscle of (A) a 3-day-old and (B) a 27-day-old worker bee.The count of nuclei under each peak and the average ploidy level are given immediately below each histogram. The reported significant reduction of ploidy with age (P < 0.01) is reflected in the reduced 8N peak and 16N peak in the older bee.

Mentions: In contrast, ploidy levels in muscle tissues decreased significantly with age. The leg muscles were replicated through almost one round (0.90) at emergence, and that level decreased significantly as workers aged (-0.0041; P < 0.05). The muscles of the thorax (i.e., flight muscles) had the second smallest levels of endoreduplication (0.59) at emergence, yet showed the most significant reduction of endopolyploidy with age (-0.0088; P < 0.001). Fig 2 shows an example of ploidy reduction in flight muscle from 0.69 at age 3 to 0.22 at age 27 post emergence. By 55 days post emergence, almost all of the cell nuclei of thoracic muscles were unreplicated (diploid), with average endoreduplication levels below that of even the neural tissues (Fig 1).


Endopolyploidy changes with age-related polyethism in the honey bee, Apis mellifera.

Rangel J, Strauss K, Seedorf K, Hjelmen CE, Johnston JS - PLoS ONE (2015)

Histograms showing fluorescence peaks centered at mean fluorescence channels 25, 50, 100, 200, and 400 produced by 2N, 4N, 8N, 16N and 32N nuclei isolated from flight muscle of (A) a 3-day-old and (B) a 27-day-old worker bee.The count of nuclei under each peak and the average ploidy level are given immediately below each histogram. The reported significant reduction of ploidy with age (P < 0.01) is reflected in the reduced 8N peak and 16N peak in the older bee.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4400096&req=5

pone.0122208.g002: Histograms showing fluorescence peaks centered at mean fluorescence channels 25, 50, 100, 200, and 400 produced by 2N, 4N, 8N, 16N and 32N nuclei isolated from flight muscle of (A) a 3-day-old and (B) a 27-day-old worker bee.The count of nuclei under each peak and the average ploidy level are given immediately below each histogram. The reported significant reduction of ploidy with age (P < 0.01) is reflected in the reduced 8N peak and 16N peak in the older bee.
Mentions: In contrast, ploidy levels in muscle tissues decreased significantly with age. The leg muscles were replicated through almost one round (0.90) at emergence, and that level decreased significantly as workers aged (-0.0041; P < 0.05). The muscles of the thorax (i.e., flight muscles) had the second smallest levels of endoreduplication (0.59) at emergence, yet showed the most significant reduction of endopolyploidy with age (-0.0088; P < 0.001). Fig 2 shows an example of ploidy reduction in flight muscle from 0.69 at age 3 to 0.22 at age 27 post emergence. By 55 days post emergence, almost all of the cell nuclei of thoracic muscles were unreplicated (diploid), with average endoreduplication levels below that of even the neural tissues (Fig 1).

Bottom Line: We found a nonsignificant increase in ploidy levels with age (P < 0.1) in the most highly endopolyploid secretory cells, the Malpighian tubules.Endopolyploidy decreased the least amount (nonsignificant) in neural (brain) cells and the stinger (P < 0.1).There was a significant reduction of endopolyploidy with age in leg (P < 0.05) and thoracic (P < 0.001) muscles.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, Texas A&M University, College Station, Texas 77843, United States of America.

ABSTRACT
Honey bees (Apis mellifera) exhibit age polyethism, whereby female workers assume increasingly complex colony tasks as they age. While changes in DNA methylation accompany age polyethism, other DNA modifications accompanying age polyethism are less known. Changes in endopolyploidy (DNA amplification in the absence of cell division) with increased larval age are typical in many insect cells and are essential in adults for creating larger cells, more copies of essential loci, or greater storage capacity in secretory cells. However, changes in endopolyploidy with increased adult worker age and polyethism are unstudied. In this study, we examined endopolyploidy in honey bee workers ranging in age from newly emerged up to 55 days old. We found a nonsignificant increase in ploidy levels with age (P < 0.1) in the most highly endopolyploid secretory cells, the Malpighian tubules. All other cell types decreased ploidy levels with age. Endopolyploidy decreased the least amount (nonsignificant) in neural (brain) cells and the stinger (P < 0.1). There was a significant reduction of endopolyploidy with age in leg (P < 0.05) and thoracic (P < 0.001) muscles. Ploidy in thoracic muscle dropped from an average of 0.5 rounds of replication in newly emerged workers to essentially no rounds of replication (0.125) in the oldest workers. Ploidy reduction in flight muscle cells is likely due to the production of G1 (2C) nuclei by amitotic division in the multinucleate striated flight muscles that are essential to foragers, the oldest workers. We suggest that ploidy is constrained by the shape, size and makeup of the multinucleate striated muscle cells. Furthermore, the presence of multiple 2C nuclei might be optimal for cell function, while higher ploidy levels might be a dead-end strategy of some aging adult tissues, likely used to increase cell size and storage capacity in secretory cells.

Show MeSH
Related in: MedlinePlus