Plant genomes: phenotypes evolving by new rules

Todd J. Vision

Department of Biology

University of North Carolina at Chapel Hill

Functional conservation of genes across distantly related plants

• GA1 (a dwarf gibberellin insensitive mutant from Arabidopsis)

• GA1 protein sequence used to identify a homolog from the grass sequence database

• Homolog shown to map to the Reduced height-1 loci in wheat and to the dwarf-8 locus in maize (Green Revolution genes)

Comparative mapping for candidate genes

Goff et al (2002) Science 296, 92

Convergent genetic architectures?

Genomic regions of foxtail millet, maize, and sorghum that carry genes for shattering of the infructescence (Devos, Plant Cell 2000)

Fruit weight 2.2 and the domestication of Solanaceous fruit crops

Frary et al (2000) Science 289, 85

Arabidopsis thaliana as a hub for plant

comparative maps

• Compact genome• Fully sequenced• Well studied

genome sizes in angiosperms

145262

367 367 372 415 439 473 560 622

907

0

250

500

750

1000me

gaba

ses

data from Arumuganathan & Earle (1991)Plant Mol Biol Rep 9:208-218

Arabidopsis

Tomato

Rice

Medicago

Stevens, P.F. (2001 onwards). Angiosperm Phylogeny Website. Version 2 August 2001.

http://www.mobot.org/MOBOT/research/APweb/.

The Arabidopsis chromosome 2-4 complex

2600

3000

3400

3800

4200

1200 1600 2000 2400 2800

chromosome 2 (5.6 Mb)

chro

mos

ome

4 (4

.6 M

b)

45

52

49

54

56

Vision et al. (2000) Science 290:2114-7.

Stacked genomic duplications in Arabidopsis

Duplication vs. multiplication

Multiple duplications generate abundant overlaps among homeologous regions

Chromosomal rearrangements

inversion reciprocal translocation

Many small duplicated regions may correspond to a single duplication event

Dating the duplication events

A B DC E F

0 50 100 150 200 Mya

0

2

4

6

8

10

12

0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9

amino acid substitution

freq

uenc

y of

blo

cks

Wikström et al (2001) Proc R Soc Lond B 268, 2211

Loss of duplicated genes creates a network of synteny

Homologous genes may be in the minority, especially after multiple duplications

Bancroft (2001) TIG 17, 89 after Ku et al (2000) PNAS 97, 9121

Mayer et al. (2001) Genome Res. 11, 1167

Rice-Arabidopsis synteny

Divergence among duplicated genes in rice

Goff et al. (2002) Science 296: 92

Why such gappy genomic alignments?

Gene deletion in new allopolyploids

• Some gene loss in duplicated genomes appears to occur gradually

• But there is now convincing evidence for gene loss (not merely silencing) immediately following synthetic tetraploidization in wheat (Kashkush et al, 2002, Genetics 160, 1651).

How to do comparative mapping among multiple taxa and in the

presence of genome duplications?

X

B C D E FA

B C D E FA

duplication

speciation

Species X Species Y

B C D E FA

A ECX X F A B DX F

Phytome: an online plant comparative mapping resource

• Integrating:– Organismal phylogeny– Gene family sequences, alignments, phylogenies– Genetic and physical maps

• Goals– Centralize

• Data collection

• Computation

– Provide• Comprehensive analysis of comparative mapping data

• An enabling interface

Dispersed gene duplications

• In our analysis, 85% of the dispersed duplicated gene pairs were not found in duplicated blocks.

• Dispersed duplications tended to co-occur on the same chromosome, and closer together, than they would if dispersed randomly.

• Lynch & Conery (2001) estimate the duplication frequency in Arabidopsis to be 2x10-3 per gene per MY and the half-life of duplicate pairs to be 23 MY. This estimate combines tandem and dispersed duplicates.

Gene order repatterning – the unknown consequences

• We know very little…• Are there blocks of gene order being actively

maintained by selection?– Self-incompatibility loci– Coordinately regulated stress-response genes

• How much phenotypic evolution is due to gene expression changes brought about by gene order rearrangements?

Acknowledgements• collaborators

– Daniel Brown (U Waterloo)– Peter Calabrese (U Southern California)– Brandon Gaut (U California Irvine)– Steven Tanksley (Cornell U)– Liqing Zhang (U Chicago)

• students– Sugata Chakravarti (UNC-CH)– Luke Huan (UNC-CH)– Dihiu Liu (UNC-CH)

• support– USDA-ARS, NSF Plant Genome