Pollen tube contents from failed fertilization contribute to seed coat initiation in Arabidopsis

Abstract

Plant seeds are essential for human beings, constituting 70% of carbohydrate resources worldwide; examples include rice, wheat, and corn. In angiosperms, fertilization of the egg by a sperm cell is required for seed formation; therefore, fertilization failure results in no seed formation, except in the special case of apomixis. Initially, plants produce many pollen grains inside the anthers; once the pollen grain is deposited onto the top of the pistil, the pollen tube elongates until it reaches the ovule. Generally, only one pollen tube is inserted into the ovule; however, we previously found that if fertilization by the first pollen tube fails, a second pollen tube could rescue fertilization via the so-called fertilization recovery system (FRS). Our previous reports also demonstrated that failed fertilization results in pollen tube-dependent ovule enlargement morphology (POEM), enlarged seeds, and partial seed coat formation if the pollen tube releases the pollen tube contents into the ovule. However, we have not determined whether all the ovules enlarge or produce seed coats if an ovule accepts the pollen tube contents. Therefore, we conducted a partial seed coat formation experiment taking into account both the FRS and POEM phenomena. Notably, the ratios of failed fertilization and the ovules with partial seed coats matched, indicating that all ovules initiate seed coat formation if the fertilization fails but the pollen tube contents enter the ovule. In addition, we confirmed that the agl62 mutant , defective in early endosperm formation, showed seed coat initiation with and without fertilization, indicating that for a normal seed coat initiation, fertilization is not required; however, for the completion of normal seed coat formation, both normal fertilization and endosperm formation are required. Further molecular evidence is required to understand these phenomena because very few factors related to FRS and POEM have been identified.

High-quality sugar production by osgcs1 rice

“…2d and Supplementary Data 3 ) are the most likely candidates directly involved in the process. In earlier studies on Arabidopsis , Kasahara, et al 11 and Liu, et al 12 , observed that PTC release alone can trigger the seed coat initiation but can not sustain ovular growth beyond 3DAP. The fundamental differences in the developmental process and function of the component tissues in rice and Arabidopsis seeds might be the underlying cause behind the disparity between their respective POEMed and POEMed-like ovules.…”

“…In previous study, we identified an important phenomenon, pollen tube-dependent ovule enlargement morphology (POEM), a new reproductive step between pollen tube guidance and fertilization 6 . Pollen tube content (PTC) release inside the ovule triggers POEM, which in turn, increases the ovule size and initiates seed coat formation without fertilization 11 , 12 . Discovery of the POEM phenomenon showed its potential applications in crop breeding for seed size increment and apomixis induction.…”

Fertilization-Defective Gametophytic Mutant Screening: A Novel Approach

“…This method is relatively quicker and precise as the researchers can determine whether any of the mutations affect fertilization and simultaneously identify the affected gamete type (FG or MG) in a single generation. It exploits the advantage of vanillin staining based on the recent findings of Beale et al (2012) ; Kasahara et al (2016) ; Liu et al (2019) , and Liu et al (2020) .…”

“…Since pollen tube content (PTC) release in the ovule triggers seed coat formation and the successful fertilization allows its continued and complete formation ( Liu et al, 2019 ), the fertilized ovules show full vanillin staining ( Figure 2A ) while those which received PTC but failed fertilization show partial staining ( Figure 2B ). The ovules lacking PTC (and fertilization), on the other hand, do not stain at all ( Figure 2C ).…”

“…Additionally, its cross with gcs1/+ (♂) (a cross equivalent to the self-cross of a fully penetrant fertilization-defective dual-gametophytic mutant) would show 37.5% seed-set. The vanillin staining would show the ratio of 3:5:0 (full:partial:no), with ~37.5 and ~62.5% seeds/ovules showing full and partial staining, respectively ( Liu et al, 2019 ). Hence, this screening approach may identify those ~4% of the mutants affecting both gametes, which would otherwise be lost during the classical screening process ( Bonhomme et al, 1998 ).…”