The evolution of plant complexity

Question 1

Plant adaptation to land

Answer 1

Land plants have gradually accumulated multiple adaptations to a terrestrial environment

see summary of innovations by Natural history museum in notes (cladogram of plant evolution)

Question 2

Several different groups manage to invade land – for some reason easier for animals than plants
Animals body plan more defined earlier on whilst plants show more variation.

Answer 2

Animals
* Metazoa originate from unicellular
sisters N635 Mya
* Many land-sea transitions
* Cambrian body plan radiation
* Body plan set in embryogenesis
* HOX and other genes important

Plants
* Land plants originate from freshwater
multicellular sisters N470 May
* Single land-sea transition
* Devonian body plan radiation
* Body plan forms post-embryonically
* Which genes were important?

Question 3

Relevance of lifecycle evolution to diversification:

Answer 3

Invasion of land showed evolution of life cycle diversification

Lineages that made it onto land have a longer diploid phase in more recent evolution

(see diagram in notes)

Question 4

Haplontic life cycle

Answer 4

The genetic regulation of haplontic life cycle progression has been studied in a clorophyte alga called chlamydomonas

Chlamydomonas is a single celled alga, but although it is single celled there are different cell types that differentiate during different life cycle stages

Vegetative cells have two distinct identities + and – which are attracted to oneanother forming heterodimers resulting spore formation

When these are exposed to environmental conditions with low nitrate, they differentiate into gametes

If plus and minus gametes are mixed, they mate- they undergo flagellar adhesion, lose their cell wall, and form a mating structure

The two cells fuse to form a quadriflagellated cell that normally differentiates into the zygote with a tough cell wall

Mature zygotes germinate in response to light and nitrogen and undergo meiosis

There is no multicellular diploid phase meiosis occurs straight away after fertilization

Recent molecular work has shown that homeodomain genes are really important in regulating cell type identity and cell cycle progression

Question 5

Control of the generational switch

Answer 5

Two key genes showing gamete-specific expression are the TALE homeoproteins (three amino acid loop extension homeodomain containing transcription factors) Gsp1 (gamete specific plus 1) in female gametes and Gsm1 (gamete specific minus 1) in male gametes.

These form heterodimers in fused gametes and trigger development of the zygote.

Zygote development involves combining the separate nuclei, absorbing the flagella and forming a resistant cell wall

Question 6

Charophyte algae are precursors of land plants

Answer 6

Members of this lineage show advanced features of multicellular complexity and some pre-existing traits transferably useful for land life.

Different tissues with division of labour

Innovations that would later become essential for life on land including: plasmodesmata, apical growth, and rhizoids

• multicellular, cell differentiation and collaboration
• apical growth and rhizome forming

Question 7

Tougher spores are required for life on land

Answer 7

Thick walled spore-like microfossils that could be resistant to desiccation have been dated to the upper Cambrian (Taylor and Strother 2009)

Unequivocal spores are found as early as the mid-Ordovician (470 MYA) (Rubenstein et al 2010)

Fossil evidence of spores are a useful microfossil to detect plant presence

Question 8

The ‘Rhynie chert’ (-420 MYA)
Early Devonian. Exceptionally preserved ecosystem of
early land plants and assæiated algae and animals

Answer 8

Entire plant fossils of early land plants are present in Scotland – probably due to an eruption that caused heavy mineral deposits
Fossil evidence for early species diversity
Variety of branched spore bearing vegetative structures

Question 9

Haplontic life-cycle: vegetative diploids

Answer 9

Chlamydomonas sometimes exists as a fee living diploid.
Might amplify the advantages of rare fertilization events in a low density aqueous environment

How did this come about?
Vegetative state can occur to increase in number before producing spores.

Haplontic to diplontic lifecycles and alteration of generations
- Zygotes undergo mitosis and form a multicellular lifecycle stage
- Lifecycle shift – diploid phase becoming more dominant

Question 10

Potential advantages of embryogenesis

Answer 10

The multiple origins of embryogenesis and sporophyte dominance suggests that it has evolutionary advantages.

It might help periodically reset developmental plans, defining developmental axes such as root and shoot necessary for upright growth in plants. (Meiosis acts as an epigenetic reset)

It might help reset accumulated epigenetic effects and allow imprinting where one parent’s alleles are preferentially expressed.

It might limit mutational burden by limiting the number of mitotic cell divisions during the lifecycle. For example, plants appear to show a trade-off between growth rate and generation time.

Question 11

Mosses show dominance of the gametophytic stage

Answer 11

Mosses are simple plants show dominant haploid stage

Reproductive gametophytes form at the top of the leafy structure

Question 12

Ferns show dominance of the sporophyte phase

Answer 12

Cooksonia (420 MYA) gametophytes and sporophytes
Sporophyte dominance was an early event - These fossilised branch structures are sporophytes and not gametophytes (not mosses)

Question 13

The rise of sporophytes

Answer 13

A dominant sporophyte generation lends many advantages to life on land. Dessication resistant gametes are required for land living, extremes of light, heat and water availability are all limiting factors of terrestrial life

Morphological advantages:
Sporophytes generate tough desiccation-tolerant and dispersable spores to promote effective reproduction on land. This compares with typically water-dependent and sometimes free-swimming gametes
Diploid sporophytes have greater environmental resilience especially under the particular stresses of life on land including drought, temperature extremes, and intense light.

Genetic advantages

Diploidy maintains more gene copies in individuals and populations
Meiosis produces genetically diverse adaptable spores (by recombination)
More variability and control of gene expression is possible through dominant-recessive gene pair interactions

Mutational impact is reduced and a greater genetic load can be tolerated as redundant gene copies are present (genes are in pairs dom/recessvie). This is particularly useful under stressful conditions likely to induce mutation.

Question 14

Other land plant innovations

Answer 14

Vascularisation for transport, lignin (to grow taller) cuticles to reduce water loss

Vascularization for water and nutrient transport allowed the invasion of drier habitats.

Lignin reinforced cells including vasculature and general biomechanical support allowing more competitive taller plants to evolve.

Cuticles to limit water loss and stomata to regulate the rate of transpiration

Question 15

Early developmental genes duplicated and diversified in plants: KNOX genes

Answer 15

*KNOX genes duplicated before plants came onto land and have had a long time to diverge in function

*KNOX genes have retained some reproductive functions, but they have also gained new functions in land plant evolution, and have been particularly imporant in the evolution of the vegetative sporophyte body.

*KNOX genes fall into two classes and the duplication giving rise to these two classes occurred before plants moved onto land.

*We can tell this because all plants from the charophyte algae right up to the seed plants have two KNOX gene copies

*Each gene clade represents species right across the land plant tree of life

*There are two KNOX gene clades

*The Class I KNOX genes and the Class II KNOX genes

Question 16

BELL homeoproteins are expressed in sporophytes

Answer 16

*BELL1 is expressed in egg cells prior to fertilization and in embryos after fertilization suggesting that it might have roles in egg and embryo development

*BELL2 has a broader expression pattern. It is expressed in eggs and in embryos, but it is also expressed in maternal tissues surrounding the egg and embryo

*For this reason only BELL1 functions were analysed

*Loss of function mutants were made by gene targeting

Question 17

BELL homeoproteins encourage sporophyte development

Answer 17

• The role for BELL1 in life cycle progression in moss was shown by overexpressing BELL1

*leafy shoots normally develop on caulonemal filaments which can be diploid

*In the BELL1 Overexpressor mutant the caulonema initiate sporophytes rather than leafy shoots.

*These look fairly like normal sporophytes they can undergo meiosis to make spores

*The sporophytes only formed on caulonemal filaments, and the authors noted that this may be because the cells in caulonemal filaments can be diploid even though they form in the gametophyte,

*This experiment tells us that BELL1 is sufficient to trigger sporophyte formation and meiosis if the cells are diploid

*Being diploid is a requirement of sporophyte development.

Question 18

KNOX homeoproteins are expressed in sporophytes

Answer 18

There are 5 KNOX genes in Physcomitrella: 3 Class 1 and 2 Class 22
Both classes of gene are most strongly expressed in sporophytes
In the sporophyte different copies are starting to specialise in different areas

Papers originally examining KNOX gene expression did not detect it in the gametophyte

Question 19

Class I KNOX homeoproteins are necessary for sporophyte development

Answer 19

Knockout mutants limit cell proliferation in the sporophyte region that normally expresses that gene family member

Knocking out individual copies of knox results in mutational defects e.g. KNOX 1 knockout results in a malformed stem

Class I KNOX functions were originally described on the basis of mutant phenotypes observe in the sporophyte generation

MKN4 and MKN5 mutants look normal

MKN2 mutant has a shorter stem than wild type plants

This arises due to a deficiency in cell proliferation in the stem in the mkn2 mutant, and leads us into the roles for KNOX genes in vascular plants

Question 20

Lifecycle variation across plants

Answer 20

(see diagram in notes)
Lineages that did not leave the sea have also changed over time so evolution is not just triggered by becoming terrestrial – other causes also

Question 21

Class I KNOX activity is necessary and sufficient for proliferation in Arabidopsis

Answer 21

KNOX have developmental importance in morphology in more recent evoloutions also:

Class I KNOX genes regulate important aspects of later sporophyte development also as seen from these loss and gain mutants in Arabidopsis

Question 22

Increase in plant size devonian -> carboniferous

Answer 22

In the Devonian era plants grew to only about 10cm tall, by the carboniferous era we see large seedless vascular lyscospids that resemble trees

Question 23

Lecture summary

Answer 23

Phylogenetic evidence is clear that plants invaded the land from single lineage of green algae, the Charophyta.

This group of algae show a haplontic lifecycle.

The dominant stage is the haploid free-living gametophyte.

Fertilisation brings together mating-type specific homeoproteins that heterodimerize and trigger development of a resistant diploid spore.

Some extant land plant lineages such as the bryophytes, show a haplodiplontic lifecycle similar to green algae where the gametophyte is dominant but a developmentally differentiated sporophyte stage is also present.

Fossil evidence is sparse until the Rhynie chert fossils 420 MYA. By this time many land plants already showed a diplontic lifecycle with a dominant diploid sporophyte stage.

Diploid sporophytes have extra genetic material to maintain and generate genetic diversity and resist mutation under the additional stresses of terrestrial life.

This lifecycle switch was achieved by introducing and increasing mitotic divisions in the spore post fertilisation and coopting sporophyte expressed genes for additional developmental innovations in this developmental stage.