Welcome to Scribd, the world's digital library. Read, publish, and share books and documents. See more
Download
Standard view
Full view
of .
Look up keyword
Like this
1Activity
0 of .
Results for:
No results containing your search query
P. 1
The land pyrenoid: A Silurian way to deal with heat and light?

The land pyrenoid: A Silurian way to deal with heat and light?

Ratings: (0)|Views: 134 |Likes:
Published by David Richardson
The Silurian way to deal with heat and light? A novel way of looking at the evolution of early land plants.
The Silurian way to deal with heat and light? A novel way of looking at the evolution of early land plants.

More info:

Categories:Types, Research, Science
Published by: David Richardson on Nov 13, 2010
Copyright:Attribution Non-commercial

Availability:

Read on Scribd mobile: iPhone, iPad and Android.
download as PDF, TXT or read online from Scribd
See more
See less

11/13/2010

pdf

text

original

 
The land pyrenoid:A Silurian way to deal with heatand light?
Richardson, D.A. (2001) –
Cambridge University 
:
Plant science Dept.
incomplete referencing 
ABSTRACT
Early Silurian land plants (450MYA), inferably similar to the extant hornwort, could have made use of a pre-existing pyrenoid CCM, (inherited from an algal ancestor), not because CO
2
was in short supply in the aerialenvironment; (7000ppm CO
2
; 20 times greater than today's CO
2
conc.), but in response to higher temperatureand more intense light conditions compared to the water column. The land CCM, in the Silurian atmospherecould have responded to high PAR as modern day hornwort CCM’s do; by increasing efficiency for CO
2
at thecost of a reduced light use efficiency; the CCM acting as - a
''light use efficiency reducer'' 
(based on results) -and in high temperatures the CCM up regulates, also increasing efficiency for CO
2
, acting as - an
''oxygenasereaction reducer'' 
- (based on results). The hornwort CCM can be likened to a primitive stomata, regulatingCO
2
uptake, in response to light, temperature and thallus water content variations. The eventual loss of thepyrenoid CCM, and the move towards a more advanced morphology, (as seen in the C
3
liverworts), meant CO
2
was no longer being pumped around the active site of Rubisco, thus early C
3
liverwort Rubisco kinetics wouldhave improved efficiency, moreover, early C
3
liverworts evolved new chloroplast architecture to deal with highPAR in a more efficient way. Also, the evolution of pores, to reduce water loss, made the early C
3
liverwortsless dependant on water to photosynthesise, than the desiccation prone solid thallus of the hornwort.
INTRODUCTION
 
Bryophyte Phylogeny
Liverworts and hornworts are a successful group of non-flowering, rootless lower plants, grouped as bryophytes. Theypossess a polykiohydric nature, namely their water contenttends to adjust to the moisture conditions of their environment(Deltoro et al 1998). This condition is markedly different fromthat of the tracheophytes, which are homohydric, where water supply (from roots) and water status are maintained bystomatal apparatus which prevent the desiccation of thephotosynthetic tissue. Unusually though, an ancient livinggroup of bryophytes named hornworts possess stomata in thesporophyte but not the gametophyte (REF).Polykiohydry in land plants appears to be a much moreancient state than homoihydry, with Mega-fossil evidence of the early land plants shown to be liverwort-like in ultra structure(Niklas 1997; Edwards et al 1998). However within the rangeof surviving orders of bryophytes, progressive specialisation of their morphology show evidence of a move towards greater control over water relations; from simple solid thallus (
Pelliaspp
.) to the more complex differentiated structures with pores(
Marchantia spp
.) that show more control over water status.In terms of the origin and evolution of early land plants,modern day bryophytes quite possibly resemble thecharacteristics of the earliest plants on land. The first goodevidence for the existence of bryophyte-like land plants(Eoembryophytes) is seen in spore tetrads (comprising four membrane-bound spores), found over a broad geographicarea in the mid-Ordovician period, 476 Myrs (Gray 1993).The combination of decay resistant walls (implying thepresence of sporopollenin) and tetrahedral configuration(implying haploid meiotic products) are further diagnostics of land plants. Further evidence lay in spore wall ultra structureand the structure of fossil cuticles from the Late Silurian andDevonian mega fossils, leading Kendrick and Crane (1997)to suggest the above palaeobotanical evidence would
 
support previous arguments that land flora during these timeswas liverwort-like. According to Kendrick and Crane (1997),land plants (embrophytes) are most closely related to the
Charophyceae
, a small group of predominantly freshwater green algae. Within this group, either 
Coleochaetales
(15living species) or 
Charales
(400 living species) or a groupcontaining both, is a sister group to land plants. Land plantmonophyly is supported by comparative morphology andgene sequences (18S cox iii).Relationships among the major basal living groups areuncertain. But the best supported hypothesis resolvesliverworts as basal and either mosses or hornworts as theliving sister group to vascular plants (tracheophytes).
From water to air 
The transition from an aqueous medium, in which theancestral
Charophyceae
group lived, to a gaseous medium,exposed the early land plants to new physical conditions.For instance, in place of the structural support of unlimitedwater the first land plants in an aerial environment faceddesiccation exposure and the compressive effects of gravity. The early thalli would have also been exposed torelatively higher photon flux density, which would previouslyhave been exponentially attenuated by a water column, anda 10
4
gain in diffusion rate of CO2 as water places suchdiffusive limits (Osmund
et al 
1982). Consequently, keyphysiological and structural adaptations, over time, neededto occur in early land plants. Development of cutins toreduce water loss probably evolved from pre-existingelements of the primary metabolism in the ancestral
charophycean
algae (REF). Additionally, photoprotectivemechanisms possibly developed to cope with higher photonfluxes in aerial environments utilizing aspects of the alreadyexisting photo respiratory pathways (Kendrick and Crane1997). However it is unknown whether the photoprotectiverole of photorespiration evolved in photosynthetic organismsin shallow water at high light intensity or in the early landplants.
Rubisco
The effect of the land invasion by early land plants probablyhad a profound effect on the carboxylating enzyme ribulose1,5 bisphosphate carboxylase / oxygenase, Rubisco, aphotosynthetic enzyme, that had evolved in an aquaticmedia for some 3,800 million years into an aerial CO2concentration during the late Ordovician early Silurian of approx. 5400 – 7000ppm CO
2
(Berner 1998), without thediffusive barriers placed on CO2 by water.Rubisco catalyses the first step of the dark reaction side of the photosynthetic reaction termed the Calvin cycle (REF).The first step of this reaction involves Rubisco covalentlyattaching CO
2
to a 5 carbon sugar, RuBP, and thesimultaneous hydrolysis of the six carbon intermediate toform 2 molecules of PGA, of which one bears the carbonintroduced from CO
2
. However, Rubisco has a poor abilityto distinguish between CO
2
from the O
2
molecule, perhapsbecause there is no formal binding site for CO
2
.Consequently, when RuBP is bound to an active site of Rubisco, it can be attacked by O
2
, producing the twoproducts; 2 – phosphoglycolate (P-glycolate) and PGA, aprocess termed an oxygenase reaction. To salvage lost Cas a result of oxygenation of RuBP, the photorespiratorycycle (evolved earlier) recycles P-glycolate to release C atan energetic cost (REF). The poor kinetic properties of Rubisco, along with diffusive limitation to the passage of CO
2
through water and cell boundary layers were all limitingfactors to photosynthesis in the aquatic medium placing astrong selection pressure towards the development of mechanisms for increasing CO
2
concentrating around theRubisco molecule, mechanisms termed, CarbonConcentrating Mechanisms (CCMs), possibly evolving 3400MYA. The effect of raising the internal CO
2
environmentusing CCMs (sometimes by 50 – 100 fold would and doescounteract the above constraints). Whether the early landplants retained the CCM is uncertain, however, an inferencemay be made to suggest a pyrenoid-based CCM was stillpresent in some, if not all, early land plants (before c3orientation), as the pyrenoid (only found in microalage) isfound also in a group of byrophytes from the Class
 Anthocerotae
.
The biophysical CCM
The most extensively studied CCMs have been incyanobacteria which use a carboxsome-based CCM, smallpolyhedral-shaped protein bodies containing both Rubiscoand the enzyme Carbonic anhydrase (CA) which catalysesthe dehydration of HCO3- to CO
2
(Badger & Andrews 1987;Bowes 1993).CAH
+
+ HCO
3-
 
CO
2
+ H
2
OIn micro algae and some hornworts, an equivalent structureto the carboxysome is the pyrenoid, a starch coatedprotinaceous structure present in the chloroplast, believed toplay a similar role (Badger 
et al 
1993). to microalage, with apyrenoid-based CCM (Pronina & Semenko 1992; Badger 1998).To summarize the makeup of an generalized CCM, 4components are needed; (1) a mechanism whereby rapidinterconversion between CO
2
and HCO
3
- can take place,
 
extracellularly and intracellularly, the latter occurring attypical stromal pH values within the Rubisco-containingcompartment or more effectively, at low pH in the thylakoidlumen; (2) a Ci-transport mechanism at plasma membrane,chloroplast envelope or both; (3) ATP energy to power Citransport; (4) a diffusion barrier to prevent CO
2
fromdiffusing away from Rubisco (Smith & Griffiths 2000). It hasbeen established that the first two features of the above listhave been shown to involve CA in a range of eukaryoticalgae and cyanobacteria which utilise CCMs and it hasrecently been suggested that CA might function as adiffusion barrier (Raven 1997).The pyrenoid structurethought to be associated with the CCM found in many microalgae (Badger 
et al 
1994; Amoroso
et al 
1998; Woods1999) and lichenised algae (Palmqvist 1993), has alsobeen observed in some species of byrophytes from theclass
 Anthocerotae
(REF). Moreover, Vaughn (1992)established, using immuno-gold labelling, that the enzymeRubisco was found within the pyrenoid structure. Smith &Griffiths (1996b), further established that
 Anthoceroscrispus
and
Phaeoceros laevis
(Smith & Griffths 2000)exhibited low compensation points, low K
0.5
and a CO
2
uptake and release pool after photosynthesis had beeninhibited, using the C-reduction cycle inhibitor,glycoladehyde, (a method term light-dark transients),revealing a CO
2
pumping mechanism termed a DissolvedInorganic Carbon pump (DIC pump). All of which have beenused as physiological CCM diagnostics in cyanobacteriaand micro algae. To date,
Phaeoceros laevis
and
 Anthoceros crispus
have been shown to possess anoperative CCM showing similar characteristics to microalgal CCMs. But why retain this ancient microalgal relic inthe aerial environment? Considering approx 450-500 millionyears ago CO
2
Concentrations were (5400 –7000ppm) or indeed independently evolve the same (or similar)mechanism, at a latter period, during a drop in atmosphericCO2?
With or without a CCM
 
It has been observed that not all species from the
 Anthocerotae
class possess a pyrenoid state (Vaughn1990). For example all genus of the multiplastidic
Megaceros
 
spp
. and two uniplastidic species,
 Anthocerosfusiformis
and
Phaeoceros coriaceus
, do not possess apyrenoid-based CCM. This is further borne out by carbonisotope studies where the delta values for 
Megacerosmoandreus
and
Megaceros endivifolis
(herbarium samples)show C3 responses. Whereas on-line measurements on
 Anthoceros crispus
and
 Anthoceros agrestis
(sporophyte)showed a C4-like response, although there is no evidenceC4 or CAM biochemistry (
 pers com
). This situation raisessome intriguing questions as to the evolutionary significanceof the "no pyrenoid condition" in uniplastidic cells of somehornworts and liverworts that have assumed a C3orientation.
Hornwort CCM variability
Hanson, Andrews and Badger (Functional Plant BiologyVolume 29 Number 2 & 3 2002)
 
examined hornwort CCMfunction by using a combined fluorometer/massspectrometer based technique to compare pyrenoid-containing (
Phaeoceros
Prosk. and
Notothylas
Sull.) andpyrenoid-lacking (
Megaceros
Campbell) hornworts, with theliverwort
Marchantia polymorpha
L. that has standard C
3
photosynthesis and a thalloid growth form similar tohornworts. They found that
Notothylas
has more CCMactivity than
Phaeoceros
, and that
Megaceros
has the leastCCM activity.
Notothylas
and
Phaeoceros
hadcompensation points from 11–13 parts per million (ppm)CO
2
, lowe
0.5
(CO
2
) than
Marchantia
, with negligiblephotorespiration, and they accumulate a pool of dissolvedinorganic carbon (DIC) between 19–108 nmol mg
 –1
chlorophyll.
Megaceros
had an intermediate compensationpoint of 31 ppm CO
2
(compared with 64 ppm CO
2
in
Marchantia
), a lower 
0.5
(CO
2
) than
Marchantia
, and somephotorespiration, but no DIC pool. They also determined thecatalytic rate of carboxylation per active site of Rubisco for all four species (
Marchantia
, 2.6 s
 –1
;
Megaceros
, 3.3 s
 –1
;
Phaeoceros,
4.2 s
 –1
;
Notothylas
4.3 s
-1
), and found thatRubisco content was 3% of soluble protein for pyrenoid-containing species, 4% for 
Megaceros
and 8% fo
Marchantia
.
Diffusive limitations
Physiological reasons for the retention of a CCM on land, or indeed its recent evolution in response to falling atmosphericCO
2
, is still unclear, as the diffusive limitations of water areno longer limiting and unlike algae they are not moving upand down a water column, facing sudden shifts in HCO
3
-and light. However, diffusive limitations might have still beenacting on the early liverwort-like plants due to heavilycuticlised solid thalli (prior to air chamber evolution), toreduce water loss. Furthermore without pores or stomata(as seen in modern day C3 liverworts) the conductance of CO
2
within the solid thallus might have been low enough torequire the retention of a CCM.Robe, Richardson & Griffiths, (unpublished) conducted adetailed comparative study to evaluate the relative costs

You're Reading a Free Preview

Download
/*********** DO NOT ALTER ANYTHING BELOW THIS LINE ! ************/ var s_code=s.t();if(s_code)document.write(s_code)//-->