The origin of morphological novelties is a long-standing problem in evolutionary biology. An understanding of this process demands the elucidation of the developmental and genetic mechanisms that produce such structures. Dr. Chaoying He’s Group has made several important progresses on the molecular mechanisms underlying the evolution of the ‘Chinese lantern’ phenotype or inflated calyx syndrome (ICS) in Physalis.
ICS is a post-floral morphological novelty in Physalis. Its origin is associated with the heterotopic expression of the MADS-box gene MPF2 in floral organs, yet the process underlying its identity remains elusive. Here, we show that MPF3, which is expressed specifically in floral tissues, encodes a euAP1 MADS-domain protein. MPF3 was primarily localized to the nucleus, and it interacted with MPF2 and some floral MADS-domain proteins to selectively bind the CArG-boxes in the MPF2 promoter. Downregulating MPF3 resulted in a dramatic elevation in MPF2 in the calyces and androecium, leading to enlarged and leaf-like floral calyces; however, the post-floral lantern was smaller and deformed. Starch accumulation in pollen was blocked. MPF3 MPF2 double knockdowns showed normal floral calyces and more mature pollen than those found in plants in which either MPF3 or MPF2 was downregulated. Therefore, MPF3 specifies calyx identity, and regulates ICS formation and male fertility through interactions with MPF2/MPF2. Furthermore, both genes were found to activate PFINV4 that encodes an invertase cleaving sucrose, a putative key gene in sugar partitioning. The novel role of the MPF3-MPF2 regulatory circuit in male fertility is integral to the origin of ICS. Our results shed light on the evolution and development of ICS in Physalis, and on the functional evolution of euAP1s in angiosperms.
This work has been published in The Plant Cell online (Zhao et al., 2013, doi: 10.1105/tpc.113.111757). This work was supported by Chinese Academy of Sciences and the National Natural Science Foundation of China.
Figure 1 The ‘Chinese Lantern’ Phenotype and the Interacting Regulatory Networks Underlying Its Development.
(Left) The ‘Chinese lantern’ phenotype or inflated calyx syndrome (ICS) in Physalis floridana is a postfloral morphological novelty. (Right) Current integrated MPF3-associated regulatory and interacting networks for ICS development in Physalis. The networks summarize knowledge gained from previous studies (He and Saedler, PNAS, 2005; He and Saedler, Plant J, 2007; He et al., Mol Biol Evol, 2007; Plant, Zhang et al., 2012) and the present work (Zhao et al., Plant Cell, 2013).
The origin of morphological novelties is a long-standing problem in evolutionary biology. An understanding of this process demands the elucidation of the developmental and genetic mechanisms that produce such structures. Dr. Chaoying He’s Group has made several important progresses on the molecular mechanisms underlying the evolution of the ‘Chinese lantern’ phenotype or inflated calyx syndrome (ICS) in Physalis.
ICS is a post-floral morphological novelty in Physalis. Its origin is associated with the heterotopic expression of the MADS-box gene MPF2 in floral organs, yet the process underlying its identity remains elusive. Here, we show that MPF3, which is expressed specifically in floral tissues, encodes a euAP1 MADS-domain protein. MPF3 was primarily localized to the nucleus, and it interacted with MPF2 and some floral MADS-domain proteins to selectively bind the CArG-boxes in the MPF2 promoter. Downregulating MPF3 resulted in a dramatic elevation in MPF2 in the calyces and androecium, leading to enlarged and leaf-like floral calyces; however, the post-floral lantern was smaller and deformed. Starch accumulation in pollen was blocked. MPF3 MPF2 double knockdowns showed normal floral calyces and more mature pollen than those found in plants in which either MPF3 or MPF2 was downregulated. Therefore, MPF3 specifies calyx identity, and regulates ICS formation and male fertility through interactions with MPF2/MPF2. Furthermore, both genes were found to activate PFINV4 that encodes an invertase cleaving sucrose, a putative key gene in sugar partitioning. The novel role of the MPF3-MPF2 regulatory circuit in male fertility is integral to the origin of ICS. Our results shed light on the evolution and development of ICS in Physalis, and on the functional evolution of euAP1s in angiosperms.
This work has been published in The Plant Cell online (Zhao et al., 2013, doi: 10.1105/tpc.113.111757). This work was supported by Chinese Academy of Sciences and the National Natural Science Foundation of China.
ICS is a post-floral morphological novelty in Physalis. Its origin is associated with the heterotopic expression of the MADS-box gene MPF2 in floral organs, yet the process underlying its identity remains elusive. Here, we show that MPF3, which is expressed specifically in floral tissues, encodes a euAP1 MADS-domain protein. MPF3 was primarily localized to the nucleus, and it interacted with MPF2 and some floral MADS-domain proteins to selectively bind the CArG-boxes in the MPF2 promoter. Downregulating MPF3 resulted in a dramatic elevation in MPF2 in the calyces and androecium, leading to enlarged and leaf-like floral calyces; however, the post-floral lantern was smaller and deformed. Starch accumulation in pollen was blocked. MPF3 MPF2 double knockdowns showed normal floral calyces and more mature pollen than those found in plants in which either MPF3 or MPF2 was downregulated. Therefore, MPF3 specifies calyx identity, and regulates ICS formation and male fertility through interactions with MPF2/MPF2. Furthermore, both genes were found to activate PFINV4 that encodes an invertase cleaving sucrose, a putative key gene in sugar partitioning. The novel role of the MPF3-MPF2 regulatory circuit in male fertility is integral to the origin of ICS. Our results shed light on the evolution and development of ICS in Physalis, and on the functional evolution of euAP1s in angiosperms.
This work has been published in The Plant Cell online (Zhao et al., 2013, doi: 10.1105/tpc.113.111757). This work was supported by Chinese Academy of Sciences and the National Natural Science Foundation of China.
Figure 1 The ‘Chinese Lantern’ Phenotype and the Interacting Regulatory Networks Underlying Its Development.
(Left) The ‘Chinese lantern’ phenotype or inflated calyx syndrome (ICS) in Physalis floridana is a postfloral morphological novelty. (Right) Current integrated MPF3-associated regulatory and interacting networks for ICS development in Physalis. The networks summarize knowledge gained from previous studies (He and Saedler, PNAS, 2005; He and Saedler, Plant J, 2007; He et al., Mol Biol Evol, 2007; Plant, Zhang et al., 2012) and the present work (Zhao et al., Plant Cell, 2013).
(Left) The ‘Chinese lantern’ phenotype or inflated calyx syndrome (ICS) in Physalis floridana is a postfloral morphological novelty. (Right) Current integrated MPF3-associated regulatory and interacting networks for ICS development in Physalis. The networks summarize knowledge gained from previous studies (He and Saedler, PNAS, 2005; He and Saedler, Plant J, 2007; He et al., Mol Biol Evol, 2007; Plant, Zhang et al., 2012) and the present work (Zhao et al., Plant Cell, 2013).