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Function and evolution of the plant MADS-box gene family

Abstract

The function of MADS-box genes in flower and fruit development has been uncovered at a rapid pace over the past decade. Evolutionary biologists can now analyse the expression pattern of MADS-box genes during the development of different plant species, and study the homology of body parts and the evolution of body plans. These studies have shown that floral development is conserved among divergent species, and indicate that the basic mechanism of floral patterning might have evolved in an ancient flowering plant.

Key Points

  • Members of the MADS-box family of developmental genes have been found in plants, animals and fungi, with plants having by far the largest number.

  • Two types of MADS-box gene (type I and type II) have been identified on the basis of the amino-acid sequences in the MADS-box domain. Only type II MADS-box genes have been analysed at the functional level.

  • MADS-box genes have a wide range of functions, in the formation of flowers, the control of flowering time and the control of vegetative development.

  • The landmark ABC model of flower organ identity states that three classes of homeotic gene, most of which encode MADS-box proteins, function in a combinatorial manner to specify regional identities in the four floral whorls.

  • Orthologous genes in different plant species have analogous functions, indicating that the underlying mechanisms that control development might be widely conserved and that MADS-box genes have had a crucial function in plant evolution.

  • The mechanism used to pattern the flower is conserved between distantly related flowering plants such as Arabidopsis and maize and might have evolved before the divergence of monocots and eudicots.

  • The analysis of MADS-box genes in further plant species will help to uncover the role of these important genes in morphological evolution.

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Figure 1: Type II MADS-box proteins.
Figure 2: Phylogeny of the MADS-box gene family.
Figure 3: The ABC model of floral organ identity.
Figure 4: Diverse morphology of different plant species: angiosperms.
Figure 5: Diverse morphology of different plant species: gymnosperm and moss.

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Acknowledgements

We thank E. R. Alvarez-Buylla and S. Liljegren for comments; S. Pelaz for help with formatting the manuscript; and T. Homma and K. Goto for communicating results before publication. M.N. received a long-term postdoctorate fellowship from the Human Frontier Science Program Organization. Work in the laboratory of M.F.Y. is supported by grants from the US Department of Agriculture, the National Science Foundation and the National Institutes of Health.

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MCM1

AG

DEF

SRF

FLC

CO

LFY

AP1

CAL

AP2

AP3

PI

SQUAMOSA

GLO

si1

ZAG1

PLE

ZMM2

FBP2

JOINTLESS

ANR1

Ubx

abd-A

MEF2

FURTHER INFORMATION

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Yanofsky lab

ENCYCLOPEDIA OF LIFE SCIENCES

Arabidopsis: flower development and patterning

Petals

Glossary

ANGIOSPERMS

Flowering seed plants.

GYMNOSPERMS

Non-flowering seed plants, for example, pine.

MONOPHYLETIC CLADE

Descendants from a single ancestral line.

EUGLENA

A motile unicellular freshwater autotrophic organism traditionally classified as a plant-like member of the kingdom Protista (algae).

TRANSFERRED DNA

(T-DNA). A region of the Ti plasmid of Agrobacterium tumefaciens that is transferred to the plant host during an infection.

MERISTEM

The undifferentiated tissue at the tips of stems and roots in which new cell division is concentrated.

ECOTYPE

A subdivision of a species that survives as a distinct population through environmental selection and reproductive isolation.

SEPAL

The green, leaf-like organs found in the first whorl of flowers.

STAMEN

The male, pollen-bearing organ of the flower.

CARPEL

A leaf-like structure that encloses the ovules and is the defining character of angiosperms. In some species, multiple carpels might be present in a compound structure, called an ovary.

EUDICOTS

These are the largest clade of angiosperms.

MONOCOTS

(Monocotyledonous plants.) Flowering plants with one cotyledon or seed leaf.

BRACT

A modified leaf that often subtends reproductive structures.

LODICULE

One of a pair of tiny scales in a grass floret, between the lemma and the fertile parts of the flower.

PALEA

The smaller of the two bracts (the other being the lemma) that encloses the stamens and pistil in a grass floret.

DETERMINACY

Destined to produce a defined number of organs. By contrast, indeterminate structures continuously produce new organs.

DICOTS

(Dicotyledenous plants.) Dicots are plants that belong to the larger subclass of angiosperms that has two seed leaves (cotyledons) in the embryo (that is, all angiosperms that are not monocots).

NECTARY

A gland that secretes a sweet fluid (nectar), commonly but not exclusively found in insect-pollinated flowers.

STIPULE

One of a pair of appendages at the base of the leaf stalk.

COSUPPRESSION

The silencing of an endogenous gene due to the presence of a homologous transgene or virus. Cosuppression can occur at the transcriptional or post-transcriptional level.

PROPHYLL

A leaf formed at the base of a shoot, usually smaller than those formed subsequently.

INFLORESCENCE

Any type of flower cluster.

GLUME

A leaf- or bract-like structure; specifically one of the two bracts at the base of the spikelet in grass flowers.

ACHLOROPHYLLOUS

Lacking chlorophyll and thus non-green.

STIGMA

The tip of a gynoecium, which provides a surface for pollen grains to attach to and germinate. The gynoecium is the seed-bearing organ of the flower, consisting of the ovary, stigma and style.

STYLE

The portion of the pistil that connects the stigma and the ovary.

OVARY

An ovule-containing organ that is derived from fused carpels.

DEHISCENCE ZONE

The region of a pod or capsule that breaks open to release the seeds.

OVULE

The structure that consists of haploid tissue (the gametophyte generation) and the surrounding diploid tissues (the integuments), which become the seed after fertilization.

DOUBLE FERTILIZATION

In higher plants, two sperm cells from the pollen grain are involved in fertilization. One fertilizes the egg to produce the zygote (embryo) and the other combines with the fusion nucleus to produce the endosperm that will nourish the developing embryo or seedling.

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Ng, M., Yanofsky, M. Function and evolution of the plant MADS-box gene family. Nat Rev Genet 2, 186–195 (2001). https://doi.org/10.1038/35056041

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