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Mosses Make Two Different Plants From the Same Genome, and a Single Gene Can Make the Difference

The views expressed are those of the author and are not necessarily those of Scientific American.


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Two plants in one. Both are mosses, but they look wildly different. Creative Commons ndrwfgg. Click image for license and link.

One of the most astonishing secrets in biology is this: every plant you see makes two different plants from the same genome. And, scientists recently reported, a single gene from an ancient, powerful lineage can make the difference.

How can such a truth be so little known? In most land plants, including conifers and flowering plants, one of the plants is tiny, and frequently hidden inside its doppelganger. But that doesn’t mean you haven’t seen them. In fact, they may have made you suffer.

Sex and Its Consequences — and Opportunities

To  understand how plants lead secret double lives, start by thinking about your own. You might think that one copy of your genes would be sufficient to get the business of making you done. But the fact is, you have two copies of every gene in your body. One was inherited from your mother, and one from your father. This two-copy situation — referred to as diploidy — was the result of the invention of sex at some hazy date in the distant past, when two-closely related cells fused, probably by accident.

The diploid-dominant life cycle. Creative Commons Menchi. Click image for license and link.

In animals, the resulting diploid cell — a zygote — goes on to divide asexually many times, forming the multicellular organism. The genome is split apart during the reductive cell division called meiosis that precedes the creation of eggs and sperm in ovaries and testes. This genome splitting prevents the chromosome copy number from spiralling out of control with successive fertilizations.

But does it necessarily follow that if two cells fuse, any resulting multicellular organism must be diploid? What if, instead of dividing asexually through mitosis as an animal zygote does, the resulting zygote immediately underwent meiosis?  Then, the resulting haploid (single-copy) cells could divide asexually to produce multicellular haploid organisms. This would be the inverse of the animal life cycle.

The haploid dominant life cycle. Creative Commons Menchi. Click image for license and link.

This is indeed the case today for land plants’ closest living relatives, the charophycean green algae (which probably resemble land plants’ ancestors), as well as some other algae and fungi.

Now, imagine what would happen if the two life cycles combined. In other words, what if, immediately after sex, meiosis was postponed, and a multicellular diploid organism grew as it does in animals. But then, instead of making eggs and sperm that must fuse to form another diploid organism*, the diploid creature made a haploid reproductive cell called a spore that simply grows asexually into a multicellular organism? When mature, this multicellular organism would then make eggs and sperm by mitosis (instead of meiosis, as in our ovaries and testes), and voila! The circle of life is complete.

The Alternation of Generations. Creative Commons Menchi. Click image for license and link.

In this lifestyle, a single copy of the genome produces one multicellular organism. And a double copy of the genome produces another. And this reproductive tango is exactly what every land plant does, along with a smattering of brown, red, and green algae who seem to have evolved the same system separately. Scientists call this “the alternation of generations“.

Two Plants, One Creature

Sometimes, the two different organisms — both with identical genes, but one with two copies — look exactly the same. This is the case for most of the red algae, a few brown algae and many of the green algae including the sea lettuce Ulva, a tissue-thin sheet only two cells thick.

And sometimes they look wildly different, which is the case for land plants and some algae. In plants and algae, the diploid organism is called the sporophyte because it makes spores. And the haploid organism is called the gametophyte, because it makes the eggs and sperm. Here’s a figure showing how different the two can look.

From Friedman 2013, Science. Click image for link.

By way of illustration, here is the life cycle of a moss.

In spite of the title, this is not, in fact, the life cycle of a "mose". Public domain. For a reason.

The thing you think of as moss is actually the gametophyte — the haploid organism.

The sporophyte — the diploid organism — is birthed in a special flask-shaped female structure after an inept moss sperm blunders inside. It physically erupts from the parent plant as it grows, taking part of it with it. The ripped-off piece of its birthplace often remains stuck to the top of the sporophyte and is called a calyptra. The sporophyte is embedded in and often nourished by its parent. It will never leave the nest.

When mature, a medieval system of caps, lids, and teeth open up at the top of the sporophyte’s spore chamber and the moss spores are released to the wind.

When it lands, the spore sprouts a collection of alga-like filaments called a protonema. Since the haploid moss — the gametophyte — likely evolved first, it still resembles green plants’ filamentous green algal ancestors. After a few weeks, leaflets begin to sprout from the protonema and grow into the moss plant we know and love.

However, mosses, along with the even more obscure liverworts and hornworts, are unlike most land plants. Every other plant that you are likely to see is a sporophyte.

As plants evolved over the past 500 million years, sporophytes have grown more and more dominant. With each new group of land plants: horsetails, ferns, cycads, conifers, and flowering plants, the gameotphyte has steadily become more and more miniscule, until in the flowering plants, it is just a few cells big.

In conifers, the female gameotphyte is a macroscopic lump of tissue inside the cone. If you’ve eaten a pine nut, you’ve eaten the haploid female gametophyte of a pine tree, with a diploid embryonic sporophyte embedded inside — a deliciously oily polyploid sandwich.

In flowering plants — broadleaf trees, grasses, flowers — the female gametophyte is only seven cells big, and is hidden deep inside the ovary of a flower. The male is the lowly pollen grain, bane of the allergic, and this is the gametophyte that can make humans suffer. Their size is wildly out of proportion to the misery they inflict. In most cases, they are only two to four cells big.

The Off Switch for a Way of Life

How is it possible for plants — and for that matter, other algae — to produce two entirely different organisms from the same bag of genes? Biologists have been puzzling over this for a long time. The picture is still far from complete, but in a recent paper in Science, scientists from Japan, Australia, and the United States discovered that it is possible to turn the sporophyte developmental program off with the flip of a single genetic switch.

The team of researchers knocked out a pair of genes called MKN1 and MKN6 in a moss called Physcomitrella patens that belongs to a group of proteins called KNOX. KNOX proteins seem to be involved in sporophyte development. To study their function, they did what biologists almost always do in this situation: they broke them to see what would happen. Biologists call organisms where they break or remove genes to see what stops working “knockout” organisms.

The gametophyte moss with the knocked-out KNOX genes looked normal and made functional eggs and sperm, which united to form embryos. But the development of their sporophyte embryos screeched to a halt about 4 weeks after fertilization. And some of these embryos sported curious filamentous buds.

When the scientists cultured these stunted but sprouty sporophytes to see what would happen, the filaments grew into a mass resembling a protonema after a week. A week after that, the protonema produced a leafy bud resembling that made by normal moss gametophytes.

C, a normal "wild type" haploid moss gametophyte sprouting from its filamentous protonema. I. The diploid wild type moss sprophyte and its normal developmental progression 7 days post-culture. J. The mutant KNOX knockout sporophyte embryo. At 7 days post culture, it has started to produce suspciously protonema-like filaments in spite of the fact it is diploid. K. The mutant sporophyte several weeks later. It has created a protonema from which a gametophyte-like bud has grown. In spite of its looks, this plant is *diploid*. Adapted from Sakakibara et al., Science, 2013. Click image for link.

But — and this can’t be underlined enough — this thing that looked like a gametophyte but sprouted from a mutant sporophyte was diploid.

Amazingly, this diploid gametophyte then went on to produce male and female sex organs at the same rate as non-mutant plants. And even more amazingly, it produced functional eggs and sperm, in spite of the fact they too were diploid. The resulting tetraploid embryos stopped developing at the same stage as the original mutant embryos.

When the scientists made single-gene knockouts, it turned out that just one of the two KNOX genes — mkn6, a transcription factor that flips target suites of genes on or off — was responsible for the changes observed all by itself. What this implies is that mkn6 represses the haploid genetic program during the diploid generation. Which means that a single gene can make the difference between two radically different-looking plants in P. patens. That, my friends, is amazing.

The Puppet Master Genes for Earth’s Large Life

Perhaps the most fascinating aspect to this story is are the KNOX genes, of which MKN6 is one, themselves. In the last 10-20 years, scientists have been discovering that plants seem to have the same sort of puppet-master developmental control genes that animals do, which was big news itself in the decades prior.

As early eukaryotes — nucleated cells, which on Earth is everything but bacteria and archaea — groped their way toward the first complex, multicellular bodies, they needed some sort of genes to specify This Goes Here, and That Goes There. In animals, these  are called HOX genes, and one of the most incredible discoveries of 20th century biology was that the very same 180-ish base pair signature DNA sequence in these genes — the famous homeobox — underlies the embryonic developmental program of everything from worms to fruit flies to humans, specifying what the various body segments will be, whether they be antennae, wings, legs, ribs, vertebrae, or tentacles.

The homeobox of Hox genes codes for a “homeodomain” protein called a transcription factor. This homeodomain transcription factor acts as a DNA binding switch that turns suites of get-stuff-done genes on or off. The same Hox gene that tells a fruit fly embryo how to segment its body tells a developing human where the parts of its brain and spinal column go. Incredibly, they also seem to line up on the chromosome in the same order that they appear in the body, as you can see here (taking a look highly recommended!).

The really big news here, at least to me, is that plants also have homeobox-containing genes, of which the KNOX transcription factors are one type. The homeobox-containing — or homeoitic — proteins seem to have evolved in the earliest eukaryotes and remain important master control genes in nearly all surviving eukaryotes today. That means genes that controlled your development have recognizable kin in plants, algae, fungi, and protists.

The original homeobox/homeotic genes may have functioned early on as regulators of the newfangled sexual cycle, but were then co-opted as they accidentally got accidentally duplicated, diversified by random mutation, and then co-opted as regulators of anatomical development in the multicellular animals, plants, algae, and fungi, the authors of a 2009 paper in Cell suggest.

The function of the majority of plant homeobox genes remains unknown, but the KNOX genes, at least, seem to be involved in regulating sporophyte development and specifying cell identity. One group of KNOX genes, for instance, immortalizes sporophyte shoot stem cells so the shoot can grow indefinitely, much like the blood stem cells in our bone marrow must remain immortal so they can produce blood throughout our lives. The other group — KNOX2, of which MKN6 is a member — suppresses the gametophyte body plan in sporophytes.

Based on what they now know, some scientists hypothesize that in the the ancestral green algal plant, the diploid organism evolved from a zygote after a chance mutation caused a delay in meiosis after fertilization. The pause afforded an opportunity for mitosis to take place. The resulting multicellular diploid organism may have initially served simply as a dormancy phase. Inadvertently, it provided a blank canvas upon which evolution went on to paint the diversity of land plants we see today with homeotic brushes, ancient genes so powerful that their mutation can cause a fruit fly to sprout a leg instead of an antenna, or a diploid moss to think it’s another plant entirely.

——————————–

*Unlike gametes, spores can just start dividing mitotically without finding a mate to make an entirely new organism. Eggs and sperm, on the other hand, must Fuse or Die (all sperm license plates should be printed with that motto).

References

Sakakibara K., Ando S., Yip H.K., Tamada Y., Hiwatashi Y., Murata T., Deguchi H., Hasebe M. & Bowman J.L. (2013). KNOX2 Genes Regulate the Haploid-to-Diploid Morphological Transition in Land Plants, Science, 339 (6123) 1067-1070. DOI:

Friedman W.E. (2013). One Genome, Two Ontogenies, Science, 339 (6123) 1045-1046. DOI:

Lee J.H., Lin H., Joo S. & Goodenough U. (2008). Early Sexual Origins of Homeoprotein Heterodimerization and Evolution of the Plant KNOX/BELL Family, Cell, 133 (5) 829-840. DOI:

Mukherjee K., Brocchieri L. & Burglin T.R. (2009). A Comprehensive Classification and Evolutionary Analysis of Plant Homeobox Genes, Molecular Biology and Evolution, 26 (12) 2775-2794. DOI:

Jennifer Frazer About the Author: Jennifer Frazer is a AAAS Science Journalism Award-winning science writer. She has degrees in biology, plant pathology/mycology, and science writing, and has spent many happy hours studying life in situ.
Nature Blog Network
Follow on Twitter @JenniferFrazer.

The views expressed are those of the author and are not necessarily those of Scientific American.





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  1. 1. squidboy6 11:01 pm 05/12/2013

    That was very good, I’m glad to have read it, thank you. A review with an update and a conclusion.

    Link to this
  2. 2. Sex & HOX genes: learning about basic reproduction | Evolution 9:58 am 05/14/2013

    [...] Mosses Make Two Different Plants From the Same Genome, and a Single Gene Can Make the Difference | T…. [...]

    Link to this
  3. 3. Hollisjeanne 9:38 pm 05/16/2013

    Terrific post, Jennifer. Thanks for presenting the latest thinking in such a readable, interesting way. Makes me wonder about insects … e.g. caterpillar and butterfly from the same genome.

    Link to this
  4. 4. Morsels for the mind – 17/5/2013 | Six Incredible Things Before Breakfast 8:04 am 05/17/2013

    [...] A two for one deal. How mosses switch between two developmental fates using a single gene. [...]

    Link to this
  5. 5. I’ve got your missing links right here (18 May 2013) – Phenomena: Not Exactly Rocket Science 11:59 am 05/18/2013

    [...] Mosses Make Two Different Plants From Same Genome: Single Gene Can Make the Difference. By Jennifer Frazer. [...]

    Link to this
  6. 6. Found while foraging (May 28, 2013) | Inspiring Science 6:04 pm 05/27/2013

    [...] Jennifer Frazer describes how plants are able to make two completely different bodies using the same genome.  I wish I’d spotted the article and written about it, but I’m happy to link to her [...]

    Link to this

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