CrRLK1L receptor‐like kinases HERK1 and ANJEA are female determinants of pollen tube reception

Abstract

Communication between the gametophytes is vital for angiosperm fertilisation. Multiple CrRLK1L-type receptor kinases prevent premature pollen tube burst, while another CrRLK1L protein, FERONIA (FER), is required for pollen tube reception in the female gametophyte. We report here the identification of two additional CrRLK1L homologues, HERCULES RECEPTOR KINASE 1 (HERK1) and ANJEA (ANJ), which act redundantly to promote pollen tube growth arrest at the synergid cells. HERK1 and ANJ localise to the filiform apparatus of the synergid cells in unfertilised ovules, and in herk1 anj mutants, a majority of ovules remain unfertilised due to pollen tube overgrowth, together indicating that HERK1 and ANJ act as female determinants for fertilisation. As in fer mutants, the synergid cell-specific, endomembrane protein NORTIA (NTA) is not relocalised after pollen tube reception; however, unlike fer mutants, reactive oxygen species levels are unaffected in herk1 anj double mutants. Both ANJ and HERK1 associate with FER and its proposed co-receptor LORELEI (LRE) in planta. Together, our data indicate that HERK1 and ANJ act with FER to mediate female-male gametophyte interactions during plant fertilisation.

Reactive Oxygen Species as Mediators of Gametophyte Development and Double Fertilization in Flowering Plants

“…This pollen tube overgrowth phenotype is very similar to that seen in mutants of synergid-expressed genes that are necessary for communication between the female and male gametophytes. Three synergid-expressed CrRLK1L genes have been implicated in pollen tube reception: FERONIA (FER), HERKULES1 (HERK1), and ANJEA (ANJ) (Galindo-trigo et al, 2020). As discussed previously in this review, the pollen tube-expressed CrRLK1L genes ANX1/2 have been directly linked to Rboh (Boisson-Dernier et al, 2013).…”

“…fer mutants have pollen tube overgrowth and do not accumulate ROS in the micropyles of ovules, consistent with the inhibitor feeding experiments and suggesting that micropylar ROS is an important component of normal pollen tube reception. However, herk1 anj double mutants have pollen tube overgrowth but still accumulate micropylar ROS ( Galindo-trigo et al., 2019 ), indicating that the link between micropylar ROS and synergid control of pollen tube behavior may be more complex than previously thought. Higher resolution imaging of ROS dynamics during pollen tube arrival to the synergid cells in fer , lre , herk1 , and anj mutants and a better understanding of the effects of ROS on pollen tube bursting are essential to further clarify the role of ROS during pollen tube reception.…”

Genome-Wide Identification of the CrRLK1L Subfamily and Comparative Analysis of Its Role in the Legume-Rhizobia Symbiosis

“…HERK and THE genes have been reported to regulate cell wall homeostasis in A. thaliana root and leaf, and HERK genes have also been reported to be essential for fertilization [ 4 , 33 ]. AtHERK1 , AtHERK2 , and AtTHE1 show highest levels of expression in rosette leaves, roots, and siliques ( Figure 5 E).…”

“…Chlorophytes lack this plant-specific RLK subfamily, indicating that it arose during the transition from chlorophytes to embryophytes, which probably occurred about 500 million years ago (mya) [ 71 ]. A feature that differentiates embryophytes from other plants is their sexual reproduction [ 71 , 72 ] and, since some CrRLK1Ls are key regulators of fertilization [ 4 , 16 , 30 , 31 , 33 , 36 ], this may link the emergence of the CrRLK1L subfamily with the advent of embryophytes. We found that bryophyte CrRLK1Ls cluster together in a unique clade (TINIA), whereas the land plant proteins are distributed among the remaining ten clades ( Figure 1 A, Figure S1, Table S2 ).…”

“…In association with FER, other CrRLK1Ls, such as HERKULES1 (HERK1), HERK2, and THESEUS1 (THE1), are involved in cell wall maintenance and cytoplasmic membrane homeostasis (Table 1) [4]. During fertilization, two CrRLK1Ls, HERK1 and ANJEA, together with FER, mediate male-female gametophyte interaction at the synergid cells (Table 1) [33]. Four other CrRLK1Ls, ANXUR1 (ANX1), ANX2, BUDDHAs PAPER SEAL1 (BUPS1), and BUPS2 are essential for preserving the integrity of the pollen tube during growth (Table 1) [30,31].…”