The Hows and Whys of Cytoplasmic
Inheritance in seed plants
H. Lloyd Mogensen
NOT ALL INHERITED CHARACTERS ARE DETERMINED BY GENES
LOCATED IN THE NUCLEUS
Some genes are passed on from parent to offspring without ever
being part of a nuclear chromosome. Where are these genes found,
and how does this non-nuclear inheritance occur?
Cytoplasmic inheritance is transmission of genes that occur outside the nucleus
Since these genes are present outside the nucleus, in the cytoplasm, they are
Mostly occurs in eukaryotes through cytoplasmic organelles – chloroplast and
mitochondria or from cellular parasites like viruses or bacteria
Also called extra-nuclear inheritance
(1) Reciprocal differences
(2) Lack of Segregation
LEAF VARIEGATION IN
• Earliest and best known example discovered by
• Phenotype of the progeny always resembled the
female parent but male made no contribution at all
to the character
• Explanation: genes concerned for are located in the
chloroplasts within the cytoplasm and not in the
nucleus and are therefore transmitted only through
female plant (maternal inheritance).
• Chloroplasts have no regular means of distribution,
i.e. equal distribution in daughter cells may not
occur. So, some branches may appear mosaic while
others green or white.
• The number of copies of organelle genome
per organelle can vary from one to many.
• A cell or organism in which all copies of
an organelle gene are the same is called
Homoplasmic or is said to exhibit
• A cell or organism in which not all copies
of an organelle gene are the same is called
Heteroplasmic or is said to exhibit
• Heteroplasmic cell can produce
heteroplasmic and homoplasmic
Random segregation of organelles during
replication – replicative segregation
(B) Loss of cytoplasmic organelles from generative cell
Examples; Nicotiana, Plumbago, Solanum
• Degeneration and/or modification of plastids.
• Mostly does not occur until the division of generative cell within the pollen
• Mitochondria and chloroplasts enclosed within ER - derived
autophagosomes which fuse with lysosome (autophagolysosome) – digestion
• Since digestion is impartial, mitochondria may be undergoing preferential
(C) Loss of cytoplasmic organelles from sperm cells
Example: Barley (Hordeum vulgare)
• In an ultrastructural study of barley sperm cell maturation within pollen
indicates that the mitochondria within the sperm cell is reduced by 50%
from the time the sperm cells are formed until pollen maturity at anthesis.
• Organelle loss results from cytoplasmic projection formations that are
(D) Exclusion of Male cytoplasm during gametic fusion
Example: Barley, Wheat
• In barley, large number of mitochondria are present in the sperm cell upto the
time of fertilization.
• Examination of embryo sacs immediately after fertilization when sperm nuclei
are positioned at the synergids, reveals presence of cytoplasmic body
appressed to the egg cell where the nucleus is likely to enter the egg.
• So what did the cytoplasmic body contain?
7 dictyosomes, 59 mitochondria, 3 plastids and a large membrane-
less vacuole but no nucleus.
• Essentially the entire cytoplasm is excluded during syngamy in Barley.
(E) Degradation of organelle DNA within generative and/or
sperm cells – Examples: Wheat, Barley, Rice
• Sometimes, structurally intact plastids and mitochondria may survive and even
be transmitted to egg cell, but they may lack DNA or possess DNA that is
greatly modified such that it is not heritable.
• Organelle DNA modification may take place during pollen maturation and may
thus lead to suppression of male cytoplasmic inheritance.
• Some of the modifications include lack of normal plastid genome products (23s
and 16s ribosomal RNA and large subunit of Rubisco enzyme) or deletions in
the chloroplast DNA.
MICROSCOPIC TECHNIQUES TO STUDY
• Disappearance of plastid and mitochondrial DNA (nucleoid) from the
generative cells during pollen maturation was studied by staining with DNA-
specific fluorochrome DAPI
DAPI stained only the generative
cell, organelle nucleoids absent
MOLECULAR TECHNIQUES TO STUDY CYTOPLASMIC
Question – Does the absence of DAPI detectable cytoplasmic DNA really mean that,
indeed, the DNA has been completely deleted??
Southern Blot Hybridization with a probe
specific for plastid DNA (rbcL gene, which
codes for large subunit of Rubisco)
Plastid specific probe
hybridized with Alfalfa
Plastid specific probe
did not hybridize with
*This experiment validated DAPI staining results
ENZYMATIC STUDIES FOR
• If cytoplasmic DNA loss occurs during pollen maturation in plants
displaying maternal cytoplasmic inheritance, perhaps the loss is due to
specific nucleases within the pollen of these species.
• Nuclease C (Ca2+ dependent nuclease purified from Chlamydomonas
reinhardtii ) is also found in plants known to inherit plastids maternally.
• Two plants – a) Lilium longiforum (showing maternal plastid
inheritance) and b) Pelargonium zonale (showing biparental
inheritance) were studied for the presence of nuclease C by SDS_PAGE.
Whereas, nucleases were found in the pollen protein extracts of L.
longiforum, they were absent from the pollen or ovary extracts of P.
• It was also found that Nuclease C content was high in the stamens of
Why is the uniparental inheritance so prevalently maternal?? Why is the
female cytoplasm not eliminated?
It would be more disadvantageous if the more aggressive and deleterious
types of plastids were transmitted through pollen because they would be
more widespread than mutations occurring in the female plant. Exception
Maternal cytoplasmic inheritance may have evolved as a mechanism that
prevents foreign or pathogenic DNA from entering the egg (alien
Reduction in sperm cytoplasm to facilitate its movement within the pollen
tube could be a reason.
Biology is a science of exceptions!!
• Development of cytoplasmic male sterility and thus
manifestation of heterosis
• New varieties generated by mutations using
organelle specific mutagens (eg. Fluorodeoxyuridine
for chloroplast DNA and Manganese ions for
mitochondrial DNA) (Ralph Bock (2001) Transgenic Plastids in
basic research and Plant Biotechnology. J. Mol. Bio 312, 425-438)
• Control of gene flow by Transgenics
i. H. Llyod Mogensen (1996) The Hows and Whys of Cytoplasmic
Inheritance in Seed Plants, American Journal of Botany 83(3)
ii. Noriko Nagata (2010) Mechanisms for independent cytoplasmic
inheritance of mitochondria and plastids in angiosperms, J. Plant Res
iii. Cytoplasmic inheritance and Evolution of Organelle Genomes, Mark F.
Sanders and John L. Bowman (Slideshare.com)