Defective pollen tube tip growth induces neo-polyploid infertility

Abstract

Genome duplication (generating polyploids) is an engine of novelty in eukaryotic evolution and a promising crop improvement tool. Yet newly formed polyploids often have low fertility. Here we report that a severe fertility-compromising defect in pollen tube tip growth arises in new polyploids of Arabidopsis arenosa . Pollen tubes of newly polyploid A. arenosa grow slowly, have aberrant anatomy and disrupted physiology, often burst prematurely, and have altered gene expression. These phenotypes recover in evolved polyploids. We also show that gametophytic (pollen tube) genotypes of two tip-growth genes under selection in natural tetraploid A. arenosa are strongly associated with pollen tube performance in the tetraploid. Our work establishes pollen tube tip growth as an important fertility challenge for neo-polyploid plants and provides insights into a naturally evolved multigenic solution.

Lectin Receptor-Like Protein Kinase OsNRFG6 is Required for Embryo Sac Development and Fertilization in Neo-Tetraploid Rice

“…During the breeding process of NTR lines, OsNRFG6 had formed an improved genotype different from the parental lines (Yu et al 2020 ). Similar mechanism has been found that improved genotypes of fertility genes helped autotetraploid Arabidopsis arenosa to adjust its defective meiosis process and pollen tube tip growth (Morgan et al 2020 , 2021 ; Westermann et al 2024 ). Thus, the non-parental allele of OsNRFG6 may play important roles in the formation of high fertility of NTR lines.…”

“…The origin of regulation for high fertility of NTR or PMeS lines might relate to those improved genotypes of key genes formed during germplasm evolution (Koide et al 2020 ). For example, the evolved autotetraploid Arabidopsis arenosa (fertile) has formed alternate alleles of important fertility genes like ASY1 , ASY2 , ACA8 , and AGC1.5 to overcome its unstable meiotic chromosome axes, aberrant crossover interference, and defective pollen tube tip growth (Morgan et al 2020 , 2021 ; Westermann et al 2024 ). Similarly, 222–324 genes with different alleles between 13 fertile NTR lines and two sterile ATR parental lines (Jackson-4x and 96025-4x) were identified in genomic comparison (Bei et al 2019 ; Yu et al 2020 , 2021b ).…”

Cytological Observation and RNA-Seq Analyses Reveal miR9564 and Its Target Associated with Pollen Sterility in Autotetraploid Rice

“…In recent years, various factors affecting autotetraploidization sterility have been identified, including meiotic genes, miRNAs, long non-coding RNA, and DNA methylation sites [ 6 , 10 , 11 , 12 , 13 , 14 , 19 , 33 , 34 ]. Among these regulators, miRNAs with variable expression patterns have been proposed as an important factor for low fertility of autotetraploid rice.…”

“…Regardless of autopolyploidy and allopolyploidy, polyploid individuals have substantial advantages in stress resistance, biosynthesis, genomic buffering capacity, biodiversity, and heterosis [ 1 , 2 , 3 ]. However, the widespread complex reproductive defects in autotetraploid plants limit their application [ 4 , 5 , 6 , 7 ]. Autotetraploid rice, resulting from doubling its diploid counterpart, represents a promising breeding germplasm, which displays high salt and heavy metal ion resistance [ 8 , 9 , 10 , 11 ].…”

Vesicle-Mediated Regulation of Pollen tube Growth inTorenia fournieri

“…To stain callose, 0.1% aniline blue was added to cultured pollen tubes. To evaluate the distribution of demethylesterified pectin, pollen tubes were stained with 0.01% (w/v) ruthenium red for 5 min and washed in PGM 5 . To assess cell membrane integrity, 2.5 μg/ml CellMask ™ Plasma Membrane Stain (Invitrogen) was applied for 5 min followed by three washes in PGM.…”