Molecular mechanism and breeding application of male-female interaction in angiosperm

In angiosperm, the male-female interaction plays a central role in generational reproduction, ensuring the continuity of the plant life cycle by bridging the sporophyte and gametophyte generations. This process is essential for the completion of alternation of generations, enabling the perpetuation of plant species on Earth. Furthermore, this interaction directly governs seed and fruit production, which constitute a primary food source for humans. Consequently, elucidating the molecular mechanisms underlying male-female interaction holds significant importance for both flowering plants and human agriculture. This study first elucidates the process of male-female interaction. The male and female gametophytes develop in distinct reproductive structures. The female gametophyte, or embryo sac, is enclosed within the ovule, which is deeply embedded in the pistil. In contrast, the male gametophyte, or pollen grain, forms within the anther and is transported to the pistil via abiotic (e.g., wind) or biotic (e.g., insect) vectors. Upon successful pollination, the pollen grain germinates a tube to deliver the male gametes (sperm cells) to the embryo sac, culminating in double fertilization. The male-female interaction initiates when pollen lands on the stigma, triggering a series of coordinated cellular and molecular events. First, pollen recognition by the stigma permits germination and subsequent penetration. The pollen tube then elongates through the stylar transmitting tissue, undergoes guided directional growth toward the ovule, and enters the micropyle under ovular guidance. Finally, upon induction by the synergid cells, the pollen tube ruptures to release the two sperm cells, leading to gamete fusion—one sperm fertilizing the egg cell to form a diploid zygote, while the other fuses with the central cell to form the endosperm, thereby completing the reproductive process. Meanwhile, the male-female interaction process is systematically classified into three critical phases: pollen (tube)-female sporophyte interaction, pollen tube-female gametophyte interaction, and sperm-female gamete interaction. For each phase, we delineate the defining biological events and summarize their molecular regulatory mechanisms, highlighting the pivotal roles of peptide signaling and receptor-like kinases in mediating intercellular communication and feedback between male and female tissues/cells. Additionally, we analyze breeding technologies derived from male-female interaction research, because male-female interaction genetically represents the transfer of genetic material between egg and sperm cells, and crop breeding fundamentally relies on the manipulation of such genetic material. Understanding these mechanisms offers direct applications in agricultural improvement. To date, based on two key principles: the molecular basis of pollen (in) compatibility and haploid induction via defective sperm-egg fusion, several breakthrough breeding technologies have been developed, including self-reproduction in Chinese cabbage, true seed production in potato, non-isolation seed production in maize and haploid induction technology (now widely applied across multiple crops). Finally, we summarize that the male-female interaction of angiosperms is a very important research field with great potential and challenge, discuss the optimization and guiding significance of male-female interaction in existing breeding techniques and its great application potential in breaking reproductive isolation, and propose emerging research directions and novel applications for leveraging male-female interaction mechanisms in crop improvement.