Abstract
For self-pollinating plants to reproduce, male and female organ development must be coordinated as flowers mature. The Arabidopsis transcription factors AUXIN RESPONSE FACTOR 6 (ARF6) and ARF8 regulate this complex process by promoting petal expansion, stamen filament elongation, anther dehiscence, and gynoecium maturation, thereby ensuring that pollen released from the anthers is deposited on the stigma of a receptive gynoecium. ARF6 and ARF8 induce jasmonate production, which in turn triggers expression of MYB21 and MYB24, encoding R2R3 MYB transcription factors that promote petal and stamen growth. To understand the dynamics of this flower maturation regulatory network, we have characterized morphological, chemical, and global gene expression phenotypes of arf, myb, and jasmonate pathway mutant flowers. We found that MYB21 and MYB24 promoted not only petal and stamen development but also gynoecium growth. As well as regulating reproductive competence, both the ARF and MYB factors promoted nectary development or function and volatile sesquiterpene production, which may attract insect pollinators and/or repel pathogens. Mutants lacking jasmonate synthesis or response had decreased MYB21 expression and stamen and petal growth at the stage when flowers normally open, but had increased MYB21 expression in petals of older flowers, resulting in renewed and persistent petal expansion at later stages. Both auxin response and jasmonate synthesis promoted positive feedbacks that may ensure rapid petal and stamen growth as flowers open. MYB21 also fed back negatively on expression of jasmonate biosynthesis pathway genes to decrease flower jasmonate level, which correlated with termination of growth after flowers have opened. These dynamic feedbacks may promote timely, coordinated, and transient growth of flower organs.
Highlights
In typical angiosperms, late in flower development, sepals open to expose the inner organs; the petals, stamen filaments, and style elongate; the anthers dehisce to release pollen; and the stigma and transmitting tract mature so as to permit pollen germination and pollen tube growth
Positive feedbacks may ensure that the development of different flower organs is coordinated and rapid, whereas negative feedbacks may allow growth to cease once flowers have opened
Jasmonates can inhibit petal expansion by activating alternative splicing of a bHLH31/ BPE/At1g59640 transcript [9,10]. arf8 mutants had enlarged petals, suggesting that ARF8 and BPE act in a common pathway [11]. These results indicate that AUXIN RESPONSE FACTOR 6 (ARF6) and ARF8 trigger anther dehiscence by promoting jasmonate production, can promote or inhibit petal growth through jasmonate-dependent pathways, and regulate other aspects of flower maturation independently of jasmonate
Summary
Late in flower development, sepals open to expose the inner organs; the petals, stamen filaments, and style elongate; the anthers dehisce to release pollen; and the stigma and transmitting tract mature so as to permit pollen germination and pollen tube growth. These events often occur quite quickly, and are transient, so that flowers open and pollinate, but stop growing. Differential growth of stamens and style or staggered timing of anther and gynoecium maturation can instead promote cross-pollination
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