Desiccation ToleranceMechanisms and Evolution

Mel Oliver and Brent Mishler

Desiccation-tolerance.

The ability to revive from the air-dried state (the air being of low relative humidity) thus experiencing protoplasmic dehydration without suffering permanent injury

Bewley and Krochko. 1982

Types of Desiccation-tolerance.

Plants whose tolerance to water loss is low. Plant structures that are adapted to withstand

desiccation and for which water loss is an expected event. - seeds.

Plants that are capable of tolerating desiccation regardless of the rate at which water loss occurs.

Plants that are capable of tolerating desiccation only if water loss is a slow process.

Desiccation-tolerant Plants.

Desiccation-tolerant ALGAE LICHENS BRYOPHYTES

Modified Desiccation-tolerant FERNS ANGIOSPERMS

Distribution of Desiccation Tolerance in the Plant Kingdom

liverwortshornworts

mosses

SelaginellaIsoetes

Lycopodium

Equisetumfernsferns

Gingko

cycads conifersgnetophytes

Angiosperms

Land Plants

Tracheophytes

Seed Plants

Oliver, Tuba and Mishler 2000

Tortula ruralis

Selaginella

Selaginella bigelovii

Polypodium virginianum

Photo Courtesy of Dr Christina Walters USDA NSSL Fort Collins

Orthodox Seeds

Distribution of Desiccation tolerance in the Angiosperms

PoaceaeCyperaceae

Velloziaceae

Liliaceae

Magnoliales

renunculids

Hamameliales

LabiataeGesneriaceae Scrophulariaceae

AngiospermsOliver, Tuba and Mishler 2000

Xerophyta villosa

Photo Courtesy of Dr. Jill Farrant and Clare Vander Willegen University of Cape Town SA

Myrothamnus flabellifolia

Craterostigma wilmsii

Xerophyta viscosa

Sporobolus stapfianus

Photos Courtesy of Dr. Dorothea Bartels University of Bonn

Craterostigma plantagineum

Dry

Rehydrated

Hydrated

Critical Parameters for Desiccation-tolerance.

Limit damage to a repairable level Maintain physiological integrity in

the dry state Mobilize repair mechanisms upon

rehydration

Bewley 1979

Essence of Desiccation-tolerance.

Testable Hypothesis

Cellular Repair

Cellular Protection

Bryophyte Model

Dry

Rehydrated

Hydrated

RAPID WATER LOSSRAPID WATER LOSSConstitutive CellularConstitutive Cellular

ProtectionProtection Induction of Recovery and RepairMechanisms

Hormone ?Hormone ?

Angiosperm Model

SLOW WATER LOSSSLOW WATER LOSSInduction ofInduction ofCellular ProtectionCellular Protection

Re-establishmentRe-establishmentProcessesProcesses

Dry

Rehydrated

Hydrated

ABAABA

Postulated Evolutionary History of Desiccation Tolerance in Land Plants

hornwortsmosses

SelaginellaIsoetes

Lycopodium

Equisetumfernsferns

Gingko

cycads conifersgnetophytes

Angiosperms

liverworts

Constitutive protection and repair

Inducible protection plus repair?

Developmentally programmedprotection - propagules

Developmentally programmed protection - spores?

Inducible protection(repair?) and laterpoikilochlorophylly

TT

SS

Loss of vegetativedesiccation tolerancein the ancestral lineageOliver, Tuba and Mishler 2000

Bryophyte Model

Dry

Rehydrated

Hydrated

RAPID WATER LOSSRAPID WATER LOSSConstitutive CellularConstitutive Cellular

ProtectionProtection Induction of Recovery and RepairMechanisms

Hormone ?Hormone ?

A B C D E F G H I J K L M N OIn1

In2

Dhy

E F G H

Tr 288 Phylogenetic Gene Search

Tr 288 Gene

GPN-Box Consensus primers

ExpectedPCR Products(Sequence forIdentity)

Tortula ruralis

Tortula sinensis

Tortula andersonii

Tortula indet NSW

Tortula amphidiacea

Tortula subaristata

Tortula caninervis

Tortula cavelii

Tortula handelii

Tortula muralis

Tortula papillosa

Calyptopogon

288

288

288

288288

288

288

288

288

288

288 288

Probable tree root

Unrooted Tortula Phylogenetic NetworkOccurance of Tr288 Orthologs

EquisetumOsmunda

Angiopteris

SequoiaSelaginella

Huperzia

IsoetesPolytrichum piliferum

Polytrichum communeFunaria

Grimmia

Tortula ruralisTortula princepsTortula muralis

ArthrocormusLeucophanes

OctoblepharumExostratum

Pterogonium

Sphagnum cuspidatumSphagnum palustre

Anthoceros fusiformisAnthoceros

MegacerosNotothylas

Blasia

AsterellaRiccia albida

Riccia atromarginataRiccia albolimbata

Riccia frostiiRiccia membranacea

Riccia sulivantiiTargionia

Lunularia

Lophocolea

algal ancestor

288288

288288

288

288288

288288Mitthyridium288

Calyptopogon288

Probable Network Root

PsilotumPsilotum

BuxbaumiaBuxbaumia

Tetraphis

HaplomitriumHaplomitrium

Unrooted “Deep Green” Phylogenetic NetworkOccurance of Tr288 Orthologs

Phylogenetic Approachto Functionality

Establishment of a correlation between the presence of a gene and a specific phenotype

Establishment of the role of a gene in the evolution of a particular phenotype

Establishment of the importance of a particular mechanism in the evolution of a particular phenotype, e.g., induced repair upon rehydration versus induced protection during drying in desiccation-tolerance

Collaboration with Brent Mishler - UC Berkeley

Deep changeDeep change in functionin function

A phylogenetically distant comparison = large background differences

A phylogenetically close comparison= low background differences

Recent ChangeRecent Change in functionin function

Increasing complexityIncreasing complexity

Ancestor-descendant comparison usingreconstructed ancestral states