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SCIENCE CHINA Life Sciences, Volume 59, Issue 1: 24-37(2016) https://doi.org/10.1007/s11427-015-4993-2

The effect of transposable elements on phenotypic variation: insights from plants to humans

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  • ReceivedNov 12, 2015
  • AcceptedDec 16, 2015
  • PublishedJan 8, 2016

Abstract

Transposable elements (TEs), originally discovered in maize as controlling elements, are the main components of most eukaryotic genomes. TEs have been regarded as deleterious genomic parasites due to their ability to undergo massive amplification. However, TEs can regulate gene expression and alter phenotypes. Also, emerging findings demonstrate that TEs can establish and rewire gene regulatory networks by genetic and epigenetic mechanisms. In this review, we summarize the key roles of TEs in fine-tuning the regulation of gene expression leading to phenotypic plasticity in plants and humans, and the implications for adaption and natural selection.


Funded by

National Natural Science Foundation of China(31210103901,31123007)

National Basic Research Program of China(2013CB835200)

State Key Laboratory of Plant Genomics(2015B0129-01)


Acknowledgment

Acknowledgements This work was supported by the National Natural Science Foundation of China (31210103901, 31123007), the National Basic Research Program of China (2013CB835200), and the State Key Laboratory of Plant Genomics (2015B0129-01). Liya Wei was supported by the China Postdoctoral Science Foundation (2015M570170).


Interest statement

Compliance and ethics The author(s) declare that they have no conflict of interest.


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  • Figure 1

    Transposable elements (TEs) regulate gene expression by genetic (A–D, blue box) or epigenetic mechanisms (E–H, red box). Black arrowheads represent transcription start sites. Rectangles represent exons (black), introns (white). Black lines indicate the upstream and downstream region of gene body.

  • Figure 2

    Transposable elements (TEs) shape gene regulatory networks by modifying transcription factor binding sites (TFBS). The yellow triangle represents a TE. Rounded rectangles represent TFBS. Orange ellipses represent transcription factors. Black rectangles represent exons and white rectangles represent introns of genes. Black lines indicate the upstream and downstream regions of the gene. The arrowhead represents the transcription start site.

  • Table 1   Effect of TEs on phenotypic variation in plants

    Regulatory mechanism

    TE classification

    Regulated gene

    Plant phenotypes

    References

    Insertional mutagenesis

    *Class II, Ac/Ds

    C

    Variation in pigmentation pattern in maize kernels

    (McClintock, 1950)

    *Class I, LTR, Dasheng

    OsCHI

    Rice gold hull and internode (gh) mutants

    (Hong et al., 2012)

    *Class II, CACTA superfamily, Cs1

    Y

    Variegated pericarp in sorghum grain

    (Chopra et al., 1999)

    *Helitron

    BrTT8

    Yellow seed coat in Brassica rapa

    (Li et al., 2012)

    *Class I and Class II

    CHS-D

    Flower color variation in morning glory

    (Clegg and Durbin, 2000, 2003)

    *Class II, Mutator

    bHLH2

    Pale flowers and ivory seeds in Ipomoea purpurea

    (Park et al., 2007)

    *Class I, Gypsy-type LTR, Gret1

    Vvmby1A

    Changes in grape skin color

    (Kobayashi et al., 2004)

    Class II, MITE

    F35H

    Changes in potato tuber skin color

    (Momose et al., 2010)

    Class I, LTR, dem1

    MdPI

    Parthenocarpic production of apple fruit

    (Yao et al., 2001)

    *Class II, Ac/Ds

    Wx

    Waxy kernels in maize

    (Wessler et al., 1986)

    *Class II, Ac/Ds

    SBEI

    Wrinkled-seed character in peas

    (Bhattacharyya et al., 1990)

    *Class I and Class II

    GBSS1

    Waxy and low-amylase types of foxtail millet

    (Kawase et al., 2005)

    *Class I, LTR, Dasheng

    GBSS

    Glutinous rice seed in Oragamochi

    (Hori et al., 2007)

    Class II, hAT family, dTok0

    FON1

    Multiple floral organs and numerous seeds in rice

    (Moon et al., 2006)

    Class II, MuDR

    ZmGE2

    Increased embryo to endosperm ratio in maize

    (Zhang et al., 2012)

    Regulatory elements

    *Class II, Mu1

    Hcf106

    White sectors on maize leaves

    (Martienssen et al., 1990)

    Class II, Harbinger

    Pr

    Purple cauliflower

    (Chiu et al., 2010)

    Class I, retrotransposon

    b1

    Maize seed color

    (Selinger and Chandler, 2001)

    *Class I, LTR, Renovator

    Pit

    Blast resistance in rice

    (Hayashi and Yoshida, 2009)

    *Class I, Copia family, Hopscotch

    tb1

    Increased apical dominance in maize

    (Studer et al., 2011)

    *Class II, hAT family, Hatvine1-rrm

    VvTFL1A

    Somatic variation in cluster shape in grapevine

    (Fernandez et al., 2010)

    Class II, MITE

    Vgt1

    Flowering time in maize

    (Salvi et al., 2007)

    Class II, MITE

    AltSB

    Aluminum tolerance in sorghum

    (Magalhaes et al., 2007)

    *Class II, MITE, mPing

    Os01g0299700, Os02g0135500, Os02g0582900

    Response to stress in rice

    (Naito et al., 2009)

    *Class I, Copia-like

    Ruby

    The accumulation of anthocyanins in blood oranges

    (Butelli et al., 2012)

    *Class I, LTR

    Wx

    Waxy kernels in maize

    (Varagona et al., 1992)

    *Class I, Copia-like, COPIA-R7

    RPP7

    Pathogen responses

    (Tsuchiya and Eulgem, 2013)

    *Class II, CACTA family

    F3H

    Flower color and seed coat in soybean

    (Zabala and Vodkin, 2007; Zabala and Vodkin, 2005)

    Rearrangement of gene structures

    *Class II, Ac

    P-oo

    Orange pericarp and cob in maize

    (Zhang et al., 2006)

    *Class I, Copia-like, Rider

    SUN

    Morphological variation of tomato fruit

    (Xiao et al., 2008)

    *Class II, hAT family,Tam3

    nivea (niv)

    Petal color in Antirrhinum

    (Coen et al., 1986; Uchiyama et al., 2013)

    Domesticated transposase genes

    *Class II, MULE

    FHY3, FAR1

    Response to light signaling in Arabidopsis

    (Lin et al., 2007)

    *Class II, MULE

    MUSTANG

    Severe developmental defects in Arabidopsis

    (Cowan et al., 2005; Joly-Lopez et al., 2012)

    *Class II, hAT-like TE

    DAYSLEEPER

    Essential for plant development in Arabidopsis

    (Bundock and Hooykaas, 2005)

    Epigenetic regulation

    Class I, SINE

    FWA

    Late-flowering in Arabidopsis

    (Fujimoto et al., 2008; Kinoshita et al., 2007)

    *Class II, MULE

    FLC

    Late-flowering in Arabidopsis

    (Liu et al., 2004)

    *Class I, LINE

    BONSAI

    Severe dwarfing in Arabidopsis

    (Saze and Kakutani, 2007; Saze et al., 2008)

    Class II, hAT family, nDart1

    OsClpP5

    Pale-yellow variegated leaves in rice seedlings

    (Tsugane et al., 2006)

    *Class II, hAT family, Gyno-hAT

    CmWIP1

    Sex determination in melon

    (Martin et al., 2009)

    *Class I, Copia-like, SORE-1

    GmphyA2

    Photoperiod insensitivity in soybean.

    (Kanazawa et al., 2009)

    *Class II, CACTA

    ZmCCT

    Attenuated photoperiod sensitivity in maize

    (Yang et al., 2013)

    *Class I, SINE

    VTE3(1)

    Vitamin E accumulation in tomato fruits

    (Quadrana et al., 2014)

    *Class I, Copia-like, Sal-T1

    FAE1

    Erucic contents in yellow mustard (Sinapis alba)

    (Zeng and Cheng, 2014)

    (To be continued on the next page)

    (Continued)

    Regulatory mechanism

    TE classification

    Regulated gene

    Plant phenotypes

    References

    Epigenetic regulation

    *Class I, Karma

    EgDEF1

    Mantled fruits in oil palm.

    (Ong-Abdullah et al., 2015)

    *Class I, LTR, Athila family

    UBP1b

    Stress-sensitivity in Arabidopsis

    (McCue et al., 2012)

    *Class II, MITE

    MAIF1

    ABA signaling and abiotic stress responses in rice

    (Yan et al., 2011)

    *Class II, MITE, En/Spm-like

    CYP76M7, OsKSL7, CYP99A3, OsCPS4, EUI

    Plant height in rice

    (Wei et al., 2014)

    *Class II, MITE

    OsGSR1, OsBR6ox

    Leaf angle in rice

    (Wei et al., 2014)

    *Class II, MITE

    ZmNAC111

    Natural variation in maize drought tolerance

    (Mao et al., 2015)

    *Class II, MITE

    RAV6

    Leaf Angle and Seed Size in Rice

    (Zhang et al., 2015b)

    *: These examples are discussed in this review.

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