Update on signaling pathways regulating polarized intercellular communication in Arabidopsis reproduction

Abstract

Cell polarity refers to the asymmetric distribution of cellular components, structure, and function within a cell. Most instances of cell polarity in plants involve single cells or groups of cells that are attached to neighboring cells by the cell wall. Flowering plant reproduction is unique because it involves intercellular signaling between a highly polarized cell, the tip-growing pollen tube, that must navigate its way through various sporophytic tissues of the pistil to find the ovules and deliver its sperm cell cargo to the female gametes deep within the pistil where double fertilization occurs to form the next generation (Johnson et al. 2019). The pollen tube's journey involves a series of cell polarity changes in single cells occurring over short time periods in response to signals from another cell type. These interactions occur between cells that have different ploidy and potentially different genotypes if the pollen comes from a different plant. The haploid male gametophyte, or pollen grain, is formed in the anther and is the product of meiosis followed by 2 rounds of mitosis to form the vegetative cell with 2 embedded sperm cells (Fig. 1) (Hafidh and Honys 2021). In most angiosperms, the haploid female gametophyte, also known as the embryo sac, is formed in the ovule and is the product of meiosis followed by 3 rounds of mitosis to form a 7-celled structure that contains 2 gametes, the egg and central cell, and accessory cells known as the synergids and antipodal cells (Fig. 1) (Hater et al. 2020). The goal of pollination is to deliver the 2 sperm cells from the male gametophyte to the 2 gametes in the female gametophyte for double fertilization (Johnson et al. 2019). This goal requires interactions between the pollen grain and a diploid, sporophytic stigma papilla cell, followed by interactions between the tip-growing pollen tube and the sporophytic cells of the stigma, style, transmitting tract, septum, and funiculus (Fig. 1). Finally, the pollen tube interacts with the highly polarized haploid synergid cells of the female gametophyte and gets the signal to release the sperm cells so that polar interactions can occur with the egg and central cell. These interactions between the different cell types result in changes in polarity and growth direction of the tip-growing pollen tube in response to polar signals from the maternal sporophytic and gametophytic cells. (See Box 1 for an overview of tip growth in pollen tubes.) A recurrent theme in these intercellular communication events is the perception of peptide ligands by polarly localized receptor-like kinases (RLKs) leading to rapid cellular events. At several stages of plant reproduction, the CrRLK1L family of malectin-like RLKs respond to RAPID ALKALINIZATION FACTOR (RALF) or other peptide ligands secreted from a different cell type (paracrine signaling) or from the same cell (autocrine signaling) to trigger signal transduction cascades that regulate pollen tube growth direction and integrity (Zhu et al. 2021). In this Update, we will discuss the latest advances in understanding the regulation of polarized pollen tube growth and intercellular signaling during plant reproduction, with an emphasis on research from the model plant Arabidopsis (Arabidopsis thaliana). Pollen tubes are highly polarized tip-growing cells. The pollen tube is a highly polarized tip-growing cell that needs to navigate the pistil to deliver the 2 sperm cells to the embryo sac. Pollen tube elongation requires a delicate balance of speed as pollen tubes that grow too quickly can burst from loss of cell wall integrity and could miss guidance cues secreted from the pistil, but pollen tubes that grow too slowly fail to fertilize ovules (Johnson et al. 2019). The features of pollen tube tip growth have been extensively reviewed (Mollet et al. 2013; Ge et al. 2019a; Johnson et al. 2019; Adhikari et al. 2020; Hayashi and Palmgren 2021; Ou and Yi 2022). Pollen tube elongation occurs at the apical region where exocytosis of vesicles drives plasma membrane expansion (Adhikari et al. 2020). This region is differentiated from the shank of the pollen tube by cell wall modifications including demethylesterification of pectin in the shank that strengthens the cell wall (Mollet et al. 2013; Adhikari et al. 2020). ROP1 functions as a major regulator of polarized exocytosis in pollen tubes and is activated by the RLKs PRK2/6 and ANX1/2 BUPS1/2 that bind to synergid secreted LUREs and pollen tube-secreted RALFs, respectively (Ou and Yi 2022). ROP effectors regulate polarized growth through regulation of the actin cytoskeleton, tip-focused Ca2+ oscillations, and ROS generation (Johnson et al. 2019; Ou and Yi 2022). Pollen tube Ca2+ channel mutants exhibit a range of phenotypes including altered Ca2+ oscillations, impaired pollen tube growth, and pollen tube discharge defects (Ge et al. 2019b; Johnson et al. 2019). ROS homeostasis is also important for maintaining pollen tube integrity during growth through the transmitting tract and may also contribute to pollen tube bursting in the embryo sac (Ge et al. 2019b). In addition, H+ oscillations at the pollen tube apex play a role in regulating cell wall plasticity and the actin cytoskeleton (Hayashi and Palmgren 2021). The regulation of pollen tube tip growth is crucial for reproduction as these signaling mechanisms allow for directional changes as the pollen tube perceives attractants, pauses in growth during pollen tube reception, and the eventual loss of integrity as the pollen tube bursts. The process of reproduction in Arabidopsis. The male gametophyte is pollen, which contains a vegetative cell and 2 sperm cells. The female gametophyte is a seven-celled structure called the embryo sac containing an egg cell, central cell, 2 synergids, and 3 antipodal cells. A pollen grain lands on a stigma and germinates a pollen tube carrying 2 sperm cells. The pollen tube grows into the stigma through the style and transmitting tract before turning towards an ovule and exiting the transmitting tract at the septum. The pollen tube continues to grow along the surface of the funiculus towards the micropylar end of the ovule as pollen tube attractants are secreted from the synergid cells. Signaling known as pollen tube reception between the receptive synergid and pollen tube mediates the pollen tube's entry into the embryo sac and bursting, fertilizing the egg and central cell. The male gametes are enclosed within the cytoplasm of the vegetative cell of the pollen grain, which is protected by a tough pollen cell wall (Hafidh and Honys 2021). This allows pollen grains to survive the harsh environments that they encounter between anther dehiscence and deposition on the stigma by pollinators, wind, or self-pollination through close proximity of the anther and stigma. The first challenge of plant reproduction is to initiate directional pollen tube growth from a dormant pollen grain so that the pollen tube can start its journey toward the female gametophyte. This process involves polarity changes in both the pollen grain and the stigma papillae cell that interacts with that pollen grain (Kandasamy et al. 1994). Upon interaction with a stigma, the pollen grain rapid and of polarity that to of a tip-growing pollen tube within in Arabidopsis (Kandasamy et al. 1994). signaling is in the perception and communication with the pollen grain to rapid The CrRLK1L and to regulate in stigma papillae cells which in the of pollen et al. 2021). interacts with the to ROS in the papillae cell through peptide known as have been in pollen et al. A 1 of these to signaling in the stigma. pollen from the and ROS and the of the papillae cell wall the pollen grain et al. 2021). The through which ROS in the rapid pollen to the that pollen grains can and pollen tubes on that ROS regulation in the stigma is the of pollen receptor-like kinases have also been in regulating pollen in in Arabidopsis. The family of to regulate pollen and 2021). The have been as extensively as the CrRLK1L the ligands signaling are will to if these are also in regulating ROS during Pollen a rapid of Ca2+ into the pollen grain and that to pollen tube et al. In pollen in a that this rapid of Ca2+ may by receptor-like from the CrRLK1L and in a with the that ligands to et al. These of with pollen phenotypes in double and mutants fail to the polarized Ca2+ in pollen and pollen tubes are to tip growth and burst et al. et al. Ge et al. 2019b; et al. et al. ANX1/2 and BUPS1/2 are polarly localized at the of pollen tubes et al. Ge et al. and are for ANX1/2 in the pollen tube tip and the of tip growth et al. also regulate pollen tube growth through interactions with that regulate of the pollen cell wall et al. et al. et al. et al. are to bind pollen tubes at the tip as as along the of the pollen tube et al. in cell wall in other of the pollen with this the is to from the ANX1/2 signaling that occurs at the pollen tube tip et al. The next polarity challenge during the interaction is to that the pollen tube grows into the transmitting tract so that it can the journey to the In the formed pollen tube the cell wall of the papillae cell and grows to the transmitting tract (Kandasamy et al. 1994). This process requires polarized of the papillae cell a process that is at the This process is in and most pollen tubes the through the papillae cell wall. as changes in papillae wall are with altered pollen tube in which pollen tubes the papillae cell of a to the transmitting This is also in a between and regulation of papillae polarity to pollen tube growth et al. 2020). communication with the stigma, pollen tubes encounter 2 different the style and the transmitting In the style of the transmitting tract cells to a in et al. and during the from the style to the transmitting tract, pollen tubes must and respond to changes in the from the in to tip of or to bursting as the pollen tube from the style to the transmitting tract, that these signaling have a function during pollen tube entry into the transmitting tract et al. 2021). Pollen tube tip growth through the tract is to by by the pistil et al. growth through the stigma, style, and transmitting tract, pollen tubes respond to signals from the pistil by that to or the to respond to signals from the ovule so that pollen tube and reception can and in pollen tubes with pollen tubes that have through the stigma and style of a pistil before on pollen a that are during pollen tube growth through the stigma and style et al. et al. 3 that are for the pollen tube for reception at the synergids et al. 2013; et al. this to in regulating pollen tube from the transmitting In Arabidopsis reproduction, 1 pollen tube the transmitting tract at the ovule and the funiculus to the micropylar to the embryo sac et al. 2022). This an that 1 pollen tube from exiting at a This is if the sperm cells from the first pollen tube double 3 of the CrRLK1L family are in the and single mutants and double mutants have a where pollen tubes from the at the same ovule et al. 2022). with other CrRLK1L signaling et al. that from the pollen tube as ligands for these on the septum. with or in the pollen tube and of these the leading to a model that the first pollen tube that from the transmitting tract an ovule and which bind to the of to signaling that other pollen tubes from exiting the transmitting tract through an The first pollen tube is to the ovules by a of and by of the synergid leading to pollen tube and the of the sperm cells next for this the first pollen tube but the sperm cells fertilize the gametes, the are the are and the at the is so that a pollen tube can to the The model 1 pollen tube the transmitting tract the that to pollen tube from the transmitting tract a A signal from the is in a in pollen tube growth polarity that the pollen tube toward the The pollen tube must navigate its way through the to the The pollen tube's from the stigma through the transmitting tract and the an funiculus interactions with diploid, sporophytic cells. The stages of plant reproduction interactions with the haploid female gametophyte, also known as the embryo sac, which is enclosed in the sporophytic cells of the In the female gametophyte is a highly polarized structure of 2 synergid an egg cell, a central cell, and 3 antipodal cells (Fig. 1). 3 rounds of the of into the cell types (Hater et al. 2020). The first female gametophytic cell type by the pollen tube is the receptive synergid cell. cells are highly polarized with a at the end and a region known as the at the micropylar end et al. and The is the entry to the embryo sac and is the of signaling between the receptive synergid cell and the pollen tube et al. et al. of signaling during pollen tube and reception contribute to the of membrane at the is by the et al. mutants have an that the of the type and are in pollen tube guidance into the et al. is also by and et al. 2020). of is in double mutants and embryo sac is with ovules a embryo sac or synergid cells that into the et al. 2020). of synergid cells is by actin and is the of the and of the central is are the of the are et al. pollen tube the synergid cells are highly polarized called LUREs are secreted from the and through the into the cells et al. and This is on signaling et al. 2020). In the is in the synergids and to the and secreted into the et al. 2020). and ovules with an that signaling et al. 2020). LUREs bind to the pollen tube which to of the pollen tube and growth toward the micropylar end of the embryo sac and also as the for a of the kinases and 1 and et al. and are another of peptide attractants secreted from the in the et al. 2019; et al. 2019). LUREs and which pollen tube are attractants et al. 2019; et al. 2019). 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The next challenge will to these signaling to during plant reproduction, growth and and to the reproduction signaling reproduction, and as for peptide ligands in a signaling process that in the pollen tube, and potentially the pistil 1). These signaling are by in over the of plant The are a family of plasma membrane localized receptor-like kinases that have with of and a et al. The family of that function as secreted peptide ligands et al. 2021). The of the family are with et al. of the Arabidopsis have been to have Ca2+ channel in or in cells et al. Finally, are to to the plasma membrane and as with or other of the CrRLK1L family et al. 2022). from the same CrRLK1L and family are different stages of interactions but and family to in In sporophytic also interacts with to ligands during and in response to and (Zhu et al. 2021). of the CrRLK1L and family it is that various of these form signaling that are the plant. Signaling in different stages of plant reproduction Signaling in different stages of plant reproduction A signaling of peptide ligands to a CrRLK1L and a Ca2+ channel is by the pollen tube to tip growth and by the female to pollen tube pollen a rapid of Ca2+ into the pollen grain is by and the pollen Ca2+ in the is pollen to a on the septum. Signaling of pollen tubes from an as a family of Ca2+ In both pollen tubes and synergids, are activated through signaling The signaling is at several stages during plant are the cellular events that to the different at the septum, pollen tube tip integrity bursting to release the sperm the Ca2+ by by the signaling to ROS that is by CrRLK1L are the Ca2+ oscillations in the synergids during pollen tube reception to regulating pollen tube tip growth to The are the plant the signaling in plants and in other plant the for that this to to and and the This by from the to and a of and to The and are of to the in this ROP1 ROP1 pollen

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