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1. A temperature-sensitive FERONIA mutant allele that alters root hair growth

   https://doi.org/10.1093/plphys/kiaa051  

   Kim, Daewon ; Yang, Jiyuan ; Gu, Fangwei ; Park, Sungjin ; Combs, Jonathon ; Adams, Alexander ; Mayes, Heather B ; Jeon, Su Jeong ; Bahk, Jeong Dong ; Nielsen, Erik ( December 2020 , Plant Physiology)

   null (Ed.)

   Abstract In plants, root hairs undergo a highly polarized form of cell expansion called tip-growth, in which cell wall deposition is restricted to the root hair apex. In order to identify essential cellular components that might have been missed in earlier genetic screens, we identified conditional temperature-sensitive (ts) root hair mutants by ethyl methanesulfonate mutagenesis in Arabidopsis thaliana. Here, we describe one of these mutants, feronia-temperature sensitive (fer-ts). Mutant fer-ts seedlings were unaffected at normal temperatures (20°C), but failed to form root hairs at elevated temperatures (30°C). Map based-cloning and whole-genome sequencing revealed that fer-ts resulted from a G41S substitution in the extracellular domain of FERONIA (FER). A functional fluorescent fusion of FER containing the fer-ts mutation localized to plasma membranes, but was subject to enhanced protein turnover at elevated temperatures. While tip-growth was rapidly inhibited by addition of rapid alkalinization factor 1 (RALF1) peptides in both wild-type and fer-ts mutants at normal temperatures, root elongation of fer-ts seedlings was resistant to added RALF1 peptide at elevated temperatures. Additionally, at elevated temperatures fer-ts seedlings displayed altered reactive oxygen species (ROS) accumulation upon auxin treatment and phenocopied constitutive fer mutant responses to a variety of plant hormone treatments. Molecular modeling and sequence comparison with other Catharanthus roseus receptor-like kinase 1L (CrRLK1L) receptor family members revealed that the mutated glycine in fer-ts is highly conserved, but is not located within the recently characterized RALF23 and LORELI-LIKE-GLYCOPROTEIN 2 binding domains, perhaps suggesting that fer-ts phenotypes may not be directly due to loss of binding to RALF1 peptides. 

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2. Changes in female function and autonomous selfing across floral lifespan interact to drive variation in the cost of selfing

   https://doi.org/10.1002/ajb2.1816  

   Spigler, Rachel B. ; Maguiña, Rossana ( April 2022 , American Journal of Botany)

   Abstract Premise Morphological and developmental changes as flowers age can impact patterns of mating. At the same time, direct or indirect costs of floral longevity can alter their fitness outcomes. This influence has been less appreciated, particularly with respect to the timing of selfing. We investigated changes in stigma events, autonomous selfing, outcross seed set capacity, and autofertility—a measure representing the potential for reproductive assurance—across floral lifespan in the mixed‐mating biennial Sabatia angularis . Methods We examined stigma morphology and receptivity, autonomous self‐pollen deposition, and seed number and size under autonomous self‐pollination and hand outcross‐pollination for flowers of different ages, from 1 d of female phase until 14 d. We compared autonomous seed production to maximal outcross seed production at each flower age to calculate an index of autofertility. Results The stigmatic lobes begin to untwist 1 d post anthesis. They progressively open, sextend, coil, and increase in receptivity, peaking or saturating at 8–11 d, depending on the measure. Autonomous seed production can occur early, but on average remains low until 6 d, when it doubles. In contrast, outcross seed number and size start out high, then decline precipitously. Consequently, autofertility increases steeply across floral lifespan. Conclusions Changes in stigma morphology and receptivity, timing of autonomous self‐pollen deposition, and floral senescence can interact to influence the relative benefit of autonomous selfing across floral lifespan. Our work highlights the interplay between evolution of floral longevity and the mating system, with implications for the maintenance of mixed mating in S. angularis . 

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3. Stigma receptors control intraspecies and interspecies barriers in Brassicaceae

   https://doi.org/10.1038/s41586-022-05640-x  

   Huang, Jiabao ; Yang, Lin ; Yang, Liu ; Wu, Xiaoyu ; Cui, Xiaoshuang ; Zhang, Lili ; Hui, Jiyun ; Zhao, Yumei ; Yang, Hongmin ; Liu, Shangjia ; et al ( February 2023 , Nature)

   Abstract Flowering plants have evolved numerous intraspecific and interspecific prezygotic reproductive barriers to prevent production of unfavourable offspring 1 . Within a species, self-incompatibility (SI) is a widely utilized mechanism that rejects self-pollen 2,3 to avoid inbreeding depression. Interspecific barriers restrain breeding between species and often follow the SI × self-compatible (SC) rule, that is, interspecific pollen is unilaterally incompatible (UI) on SI pistils but unilaterally compatible (UC) on SC pistils 1,4–6 . The molecular mechanisms underlying SI, UI, SC and UC and their interconnections in the Brassicaceae remain unclear. Here we demonstrate that the SI pollen determinant S -locus cysteine-rich protein/ S -locus protein 11 (SCR/SP11) 2,3 or a signal from UI pollen binds to the SI female determinant S -locus receptor kinase (SRK) 2,3 , recruits FERONIA (FER) 7–9 and activates FER-mediated reactive oxygen species production in SI stigmas 10,11 to reject incompatible pollen. For compatible responses, diverged pollen coat protein B-class 12–14 from SC and UC pollen differentially trigger nitric oxide, nitrosate FER to suppress reactive oxygen species in SC stigmas to facilitate pollen growth in an intraspecies-preferential manner, maintaining species integrity. Our results show that SRK and FER integrate mechanisms underlying intraspecific and interspecific barriers and offer paths to achieve distant breeding in Brassicaceae crops. 

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4. Synergid cell calcium oscillations refine understanding of FERONIA/LORELEI signaling during interspecific hybridization

   https://doi.org/10.1007/s00497-023-00483-6  

   Ponvert, Nathaniel ; Johnson, Mark A. ( November 2023 , Plant Reproduction)

   Pollen tubes from closely related species and mutants lacking pollen tube MYB transcription factors are able to initiate FER/LRE-dependent synergid cell calcium oscillations.

   Reproductive isolation leads to the evolution of new species; however, the molecular mechanisms that maintain reproductive barriers between sympatric species are not well defined. In flowering plants, sperm cells are immotile and are delivered to female gametes by the pollen grain. After landing on the stigmatic surface, the pollen grain germinates a polarized extension, the pollen tube, into floral tissue. After growing via polar extension to the female gametes and shuttling its cargo of sperm cells through its cytoplasm, the pollen tube signals its arrival and identity to synergid cells that flank the egg. If signaling is successful, the pollen tube and receptive synergid cell burst, and sperm cells are released for fusion with female gametes. To better understand cell–cell recognition during reproduction and how reproductive barriers are maintained between closely related species, pollen tube-initiated synergid cell calcium ion dynamics were examined during interspecific crosses. It was observed that interspecific pollen tubes successfully trigger synergid cell calcium oscillations—a hallmark of reproductive success—but signaling fails downstream of key signaling genes and sperm are not released. This work further defines pollen tube–synergid cell signaling as a critical block to interspecific hybridization and suggests that the FERONIA/LORELEI signaling mechanism plays multiple parallel roles during pollen tube reception.

    

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5. Stigma shape shifting in sages ( Salvia : Lamiaceae): hummingbirds guided the evolution of New World floral features

   https://doi.org/10.1093/botlinnean/boab096  

   Kriebel, Ricardo ; Drew, Bryan T ; González-Gallegos, Jesús G ; Celep, Ferhat ; Antar, Guilherme M ; Pastore, José Floriano ; Uría, Rolando ; Sytsma, Kenneth J ( December 2021 , Botanical Journal of the Linnean Society)

   Abstract A fundamental question in evolutionary biology is how clades of organisms exert influence on one another. The evolution of the flower and subsequent plant/pollinator coevolution are major innovations that have operated in flowering plants to promote species radiations at a variety of taxonomic levels in the Neotropics. Here we test the hypothesis that pollination by Neotropical endemic hummingbirds drove the evolution of two unique stigma traits in correlation with other floral traits in New World Salvia (Lamiaceae). We examined morphometric shapes of stigma lobing across 400 Salvia spp., scored presence and absence of a stigma brush across Salvia, and used a suite of phylogenetic comparative methods to detect shape regime shifts, correlation of trait shifts with BayesTraits and phylogenetic generalized least square regressions, and the influence of scored pollinators on trait evolution using OUwie. We found that a major Neotropical clade of Salvia evolved a correlated set of stigma features, with a longer upper stigma lobe and stigmatic brush, following an early shift to hummingbird pollination. Evolutionary constraint is evident as subsequent shifts to bee pollination largely retained these two features. Our results support the hypothesis that hummingbirds guided the correlative shifts in corolla, anther connective, style and stigma shape in Neotropical Salvia, despite repeated shifts back to bee pollination. 

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