Plant Male Fertility Research Articles

ZmMS1/ZmLBD30-orchestrated transcriptional regulatory networks precisely control pollen exine development

Because of its significance for plant male fertility and, hence, direct impact on crop yield, pollen exine development has inspired decades of scientific inquiry. However, the molecular mechanism underlying exine formation and thickness remains elusive. In this study, we identified that a previously unrecognized repressor, ZmMS1/ZmLBD30, controls proper pollen exine development in maize. Using an ms1 mutant with aberrantly thickened exine, we cloned a male-sterility gene, ZmMs1, which encodes a tapetum-specific lateral organ boundary domain transcription factor, ZmLBD30. We showed that ZmMs1/ZmLBD30 is initially turned on by a transcriptional activation cascade of ZmbHLH51-ZmMYB84-ZmMS7, and then it serves as a repressor to shut down this cascade via feedback repression to ensure timely tapetal degeneration and proper level of exine. This activation-feedback repression loop regulating male fertility is conserved in maize and sorghum, and similar regulatory mechanism may also exist in other flowering plants such as rice and Arabidopsis. Collectively, these findings reveal a novel regulatory mechanism of pollen exine development by which a long-sought master repressor of upstream activators prevents excessive exine formation.

A transposon surveillance mechanism that safeguards plant male fertility during stress.

Although plants are able to withstand a range of environmental conditions, spikes in ambient temperature can impact plant fertility causing reductions in seed yield and notable economic losses1,2. Therefore, understanding the precise molecular mechanisms that underpin plant fertility under environmental constraints is critical to safeguarding future food production3. Here, we identified two Argonaute-like proteins whose activities are required to sustain male fertility in maize plants under high temperatures. We found that MALE-ASSOCIATED ARGONAUTE-1 and -2 associate with temperature-induced phased secondary small RNAs in pre-meiotic anthers and are essential to controlling the activity of retrotransposons in male meiocyte initials. Biochemical and structural analyses revealed how male-associated Argonaute activity and its interaction with retrotransposon RNA targets is modulated through the dynamic phosphorylation of a set of highly conserved, surface-located serine residues. Our results demonstrate that an Argonaute-dependent, RNA-guided surveillance mechanism is critical in plants to sustain male fertility under environmentally constrained conditions, by controlling the mutagenic activity of transposons in male germ cells.

INDUCER OF CBF EXPRESSION 1 is a male fertility regulator impacting anther dehydration in Arabidopsis.

INDUCER OF CBF EXPRESSION 1 (ICE1) encodes a MYC-like basic helix-loop-helix (bHLH) transcription factor playing a critical role in plant responses to chilling and freezing stresses and leaf stomata development. However, no information connecting ICE1 and reproductive development has been reported. In this study, we show that ICE1 controls plant male fertility via impacting anther dehydration. The loss-of-function mutation in ICE1 gene in Arabidopsis caused anther indehiscence and decreased pollen viability as well as germination rate. Further analysis revealed that the anthers in the mutant of ICE1 (ice1-2) had the structure of stomium, though the epidermis did not shrink to dehisce. The anther indehiscence and influenced pollen viability as well as germination in ice1-2 were due to abnormal anther dehydration, for most of anthers dehisced with drought treatment and pollen grains from those dehydrated anthers had similar viability and germination rates compared with wild type. Accordingly, the sterility of ice1-2 could be rescued by ambient dehydration treatments. Likewise, the stomatal differentiation of ice1-2 anther epidermis was disrupted in a different manner compared with that in leaves. ICE1 specifically bound to MYC-recognition elements in the promoter of FAMA, a key regulator of guard cell differentiation, to activate FAMA expression. Transcriptome profiling in the anther tissues further exhibited ICE1-modulated genes associated with water transport and ion exchange in the anther. Together, this work reveals the key role of ICE1 in male fertility control and establishes a regulatory network mediated by ICE1 for stomata development and water movement in the anther.

Molecular Control of Male Fertility for Crop Hybrid Breeding.

In many plant species, male-sterile female lines with cytoplasmic male sterility (CMS) or nuclear-controlled environment-sensitive genic male sterility (EGMS) have long been used to efficiently produce hybrids that harness hybrid vigor or heterosis. However, the underlying molecular mechanisms for these applications have only recently been uncovered in a few species. We provide here an update on the understanding of cytoplasmic-nuclear communication based on the discovery of mitochondrial CMS genes and their corresponding nuclear fertility determinants. Recent findings that uncover diverse mechanisms such as epigenetic, transcriptional, and post-transcriptional controls of EGMS by temperature and photoperiod signals are also reviewed. Furthermore, translational research that applies basic knowledge of plant male fertility control to hybrid seed production practice is highlighted.

Efficient plant male fertility depends on vegetative nuclear movement mediated by two families of plant outer nuclear membrane proteins.

Increasing evidence suggests that nuclear migration is important for eukaryotic development. Although nuclear migration is conserved in plants, its importance for plant development has not yet been established. The most extraordinary plant nuclear migration events involve plant fertilization, which is starkly different from that of animals. Instead of evolving self-propelled sperm cells (SCs), plants use pollen tubes to deliver SCs, in which the pollen vegetative nucleus (VN) and the SCs migrate as a unit toward the ovules, a fundamental but barely understood process. Here, we report that WPP domain-interacting proteins (WIPs) and their binding partners the WPP domain-interacting tail-anchored proteins (WITs) are essential for pollen nuclear migration. Loss-of-function mutations in WIT and/or WIP gene families resulted in impaired VN movement, inefficient SC delivery, and defects in pollen tube reception. WIPs are Klarsicht/ANC-1/Syne-1 Homology (KASH) analogs in plants. KASH proteins are key players in animal nuclear migration. Thus, this study not only reveals an important nuclear migration mechanism in plant fertilization but also, suggests that similar nuclear migration machinery is conserved between plants and animals.

The F-box protein COI1 functions upstream of MYB305 to regulate primary carbohydrate metabolism in tobacco (Nicotiana tabacum L. cv. TN90).

Jasmonate (JA) plays an important role in regulating plant male fertility and secondary metabolism, but its role in regulating primary metabolism remains unclear. The F-box protein CORONATINE INSENSITIVE 1 (COI1) is a critical component of the JA receptor, and mediates JA-signalling by targeting JASMONATE ZIM-domain (JAZ) proteins for proteasomal degradation in response to JA perception. Here, we found that RNA interference-mediated knockdown of NtCOI1 in tobacco (Nicotiana tabacum L. cv. TN90) recapitulated many previously observed phenotypes in coi1 mutants, including male sterility, JA insensitivity, and loss of floral anthocyanin production. It also affected starch metabolism in the pollen, anther wall, and floral nectary, leading to pollen abortion and loss of floral nectar. Transcript levels of genes encoding starch metabolism enzymes were significantly altered in the pollen, anther wall, and floral nectary of NtCOI1-silenced tobacco. Changes in leaf primary metabolism were also observed in the NtCOI1-silenced tobacco. The expression of NtMYB305, an orthologue of MYB305 previously identified as a flavonoid metabolic regulator in Antirrhinum majus flowers and as a floral-nectar regulator mediating starch synthesis in ornamental tobacco, was extremely downregulated in NtCOI1-silenced tobacco. These findings suggest that NtCOI1 functions upstream of NtMYB305 and plays a fundamental role in coordinating plant primary carbohydrate metabolism and correlative physiological processes.

A battle between genomes in plant male fertility

Analyses of a new male sterility gene from a well-known rice cytoplasmic sterile line reveal inhibition of a nucleus-encoded protein and counteractions by nuclear fertility restorer factors. The existence of these genes in wild rice populations suggests that they may confer selective advantages.

Influence of water availability on fertility restoration of CMS lines with the ‘M35’, A4 and ‘9E’ CMS‐inducing cytoplasms of sorghum

AbstractMale fertility restoration in new types of sorghum cytoplasmic male sterility‐inducing cytoplasms (A4, ‘9E’, ‘M35’), characterized by the formation of non‐dehiscent anthers, is difficult. Lines with fertility‐restorer genes for these unique cytoplasms do occur, but rarely, and when found tend to be unstable in their inheritance and expression. The aim of this research was to explore reasons for this instability. Seven lines in three unique cytoplasms, ‘9E’, A4 and ‘M35’, and six lines that restore with these cytoplasms were grown at the Agricultural Research Institute for South‐East Region in Saratov, Russia from 1993 to 2004. Levels of male fertility restoration and various environmental factors were recorded. It is reported that for sorghum hybrids in the A4, ‘9E’ and ‘M35’ male‐sterile cytoplasms, the level of plant male fertility is determined by the level of water available to plants during anther and pollen formation that which ‘switches on’ the expression of fertility‐restoring genes, and is possibly involved in an unusual type of male fertility inheritance in these cytoplasms. The creation of reliable line‐fertility restorers capable of the restoration of male fertility of F1 hybrids in ‘M35’ cytoplasm under conditions of water stress is also reported. Current research explore mechanisms involved possible in responses to water levels at various growth stages and their influence on fertility within these cytoplasms.