A Regulatory Network for Coordinated Flower Maturation

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.

A bHLH-Type Transcription Factor, ABA-INDUCIBLE BHLH-TYPE TRANSCRIPTION FACTOR/JA-ASSOCIATED MYC2-LIKE1, Acts as a Repressor to Negatively Regulate Jasmonate Signaling inArabidopsis

“…During stamen development, auxin and GA stimulate the expression of the JA biosynthetic gene DAD1 (Yu et al, 2004;Nagpal et al, 2005;Ito et al, 2007;Cheng et al, 2009;Tabata et al, 2010;Reeves et al, 2012). Elevated biosynthesis of JA in anthers leads to expression of MYB21, MYB24, and MYB57, which are involved in filament elongation, pollen maturation, and anther dehiscence (Mandaokar et al, 2006;Mandaokar and Browse, 2009;Reeves et al, 2012).…”

“…Elevated biosynthesis of JA in anthers leads to expression of MYB21, MYB24, and MYB57, which are involved in filament elongation, pollen maturation, and anther dehiscence (Mandaokar et al, 2006;Mandaokar and Browse, 2009;Reeves et al, 2012). The expression of MYB21 was significantly suppressed in coi1-1 mutants, indicating that JA-Ile perception by COI1 and subsequent JA signal transduction is necessary for induction of MYB21 in male organs Reeves et al, 2012). The expression of MYB21 and MYB24 in opr3 stamens is induced within 2 h and reaches a peak at 8 h after JA treatment, but JAM1 and MYC2 induction occurs earlier than that (Mandaokar et al, 2006).…”

“…These results suggest that the mechanisms that promote JA responses in flower organs are different from those in other organs. In addition, recent reports showed that MYB21 and MYB24 directly interact with JAZs, which attenuate their transcriptional functions , and that MYB21 negatively regulates expression of JA biosynthetic enzyme genes to decrease JA levels in the flower (Reeves et al, 2012), indicating that JA-mediated male fertility is regulated by a complicated transcriptional network.…”

Developmental Defects Mediated by the P1/HC-Pro Potyviral Silencing Suppressor Are Not Due to Misregulation of AUXIN RESPONSE FACTOR 8

“…The arf8-6 line is the University of Wisconsin T-DNA line WiscDsLox324F09 (Goetz et al, 2006). The arf8-8 line has an ethyl methane sulfonate-generated G to A mutation in a splice acceptor site in ARF8 (Reeves et al, 2012). The arf8-3 null mutation line has a T-DNA insertion in the transcribed region of ARF8 (Nagpal et al, 2005).…”

“…Hemizygous and homozygous arf8-8 plants were genotyped using the PCR primers and EcoNI digestion of the PCR product as described previously (Reeves et al, 2012). For hemizygous and homozygous arf8-6 genotyping, the T-DNA primer LB (59-AACGTCCGCAATGTGTTATTAAGTTGTC-39) was used with primers ARF8-6LP (59-CGAGGAAAGGTGAAACCTAC-39) and ARF8-6RP (59-AGCTGTCAACATCTGGATTGG-39).…”