Molecular mechanisms underlying plant environment-sensitive genic male sterility and fertility restoration

Dongdong Liu; Jianxin Shi; Wanqi Liang; Dabing Zhang; Dongdong Liu; Jianxin Shi; Wanqi Liang; Dabing Zhang

doi:10.48130/SeedBio-2023-0013

Figures (5) Tables (1)

Figure 1.
TMS10/TMS10L, OsTMS5 buffer temperature changes to maintain rice male fertility. (a) In WT, TMS10 and TMS10L relay extracellular signals via substrate phosphorylation (P) to safeguard male fertility at high and low temperatures (HT/LT). In the tms10 mutant at HT, TMS10L is poorly expressed and signals cannot be transduced, resulting in abnormal tapetum degradation and male sterility. At LT, however, TMS10L can restore signal transduction to recover male fertility of the tms10 mutant. The tms10 tms10l double mutant is completely sterile at all temperatures. Red crosses indicate loss of function. (b) In WT, OsTMS15, interacting with its ligand OsTDL1A, initiates tapetum development for pollen formation at HT or LT. In the ostms15 mutant with an amino acid substitution in its TIR motif, the interaction between mTIR and OsTDL1A is reduced, leading to defective tapetum function and male sterility at HT. LT can enhance the interaction and restore tapetum function and male fertility of ostms15 mutant. The knockout line ostms15-cr has no tapetum and is completely sterile at both HT and LT conditions. Os, Oryza sativa (rice).
Figure 2.
CSA and CSA2 are a pair of R2R3 MYB transcription factors in rice mediating male fertility adaptation to photoperiod. CSA is a key regulator under short-day (SD) conditions while CSA2 a major regulator under long-day (LD) conditions, both influencing sugar partitioning to the anther. In the csa mutant under SD, downstream target genes, including MST8, are not activated, leading to defective sugar partitioning and male sterility; under LD conditions, CSA2 can restore fertility of the csa mutant. In the csa2 mutant under LD, the loss of CSA2 function reduces activation of downstream target genes, leading to male semi-sterility; while CSA works under SD to restore male fertility. Red crosses indicate loss of function.
Figure 3.
PHD finger proteins OsMS1 and GmMS3 affect temperature- or photoperiod-sensitive adaption of plant male reproduction in rice and soybean, respectively. (a) Schematic showing domains of plant homeodomain (PHD) finger proteins. Truncation of PHD in gmms3 leads to PGMS in soybean. The L301P substitution in the OsMS1^wenmin1 LXXLL (L, leucine; X, any amino acid) motif leads to TGMS in rice. Deletion of the LXXLL and PHD domains in OsMS1/GmMS3 leads to complete male sterility. (b) Short-day (SD) conditions do not induce the expression of gmms3, leading to abnormal carbohydrate metabolism in anthers and male sterility. Long-day (LD) conditions is sufficient to activate gmms3 and restore male fertility. Red crosses indicate loss of function. (c) At high temperature (HT), OsMS1^wenmin1 is expressed at low levels and distributed across both cytoplasm and nucleus, so nuclear concentration is insufficient to activate target genes, e.g., EAT1, leading to male sterility. At low temperature (LT), OsMS1^wenmin1 is expressed at higher levels and concentrated appropriately in the nucleus to restore male fertility. Os, Oryza sativa (rice); Gm, Glycine max (soybean); NLS, nuclear localization signal.
Figure 4.
Pollen coat composition affects fertility at low humidity in rice and Arabidopsis OsOCS12/OsPTS1 influences long-chain fatty acid transport, and OSGL1-4/OsCER1, HMS1/OsCER2, and AtCER1, AtCER2, AtCER2L2, AtCER3, AtCER6 play roles in VLC fatty acid biosynthesis. Mutation in these genes (singly or in pairs) compromises pollen coat composition to reduce adhesion and hydration under low humidity (LH). At, Arabidopsis thaliana; HH, high humidity; VLC, very long chain.
Figure 5.
Slow development and delay in pectin wall degradation can restore fertility in Arabidopsis pollen wall mutants. Low-temperature (LT), short-day (SD), low-light intensity (LLI), and the res1 mutation can slow development of pollen to recover male fertility in Arabidopsis lines defective in pollen wall formation. The res2 mutation delays pectin wall degradation, providing extra protection for developing pollen in pollen-defective mutants. Red crosses indicate loss of function.

Species	Gene name	Gene ID	Gene product	Type of EGMS	Pathway	Reference
Arabidopsis	ACOS5	At1g62940	acyl-CoA synthetase 5	P/TGMS	Pollen exine formation	[36,38]
	RVMS	At4g10950	GDSL lipase	P/TGMS	Pollen nexine formation	[36,38]
	CalS5	At2g13680	callose synthase 5	P/TGMS	Pollen exine patterning	[36,38]
	RPG1/SWEET8	At5g40260	SWEET8	TGMS	Pollen nexine formation	[34,35,38, 111,112]
	CYP703A2	At1g01280	cytochrome P450 703A2	P/TGMS	Pollen exine formation	[36,38]
	ABCG26	At3g13220	ATP-binding cassette transporter G26	TGMS	Pollen exine formation	[38]
	TMS1	At3g08970	HSP40	TGMS	Growth of pollen tubes, unfolded protein response	[113,114]
	NPU	At3g51610	ATP-dependent helicase/deoxyribonuclease subunit B	P/TGMS	Pollen primexine deposition	[36]
	IRE1A IRE1B	At2g17520 At5g24360	IRE	TGMS	Pollen coat formation, unfolded protein response	[115]
	AtSec62	At3g20920	Translocation protein	TGMS	Protein translocation and secretion	[116]
	PEAMT	At3g18000	S-adenosyl-l-methionine: phosphoethanolamine N-methyltransferase	TGMS	Signal transduction	[117]
	AtPUB4	At2g23140	E3 ligase	TGMS	Protein degeneration	[118]
	COI1	LOC9315901	F box protein	TGMS	Protein degeneration	[119]
	ICE1	At3g26744	MYC-like bHLH transcriptional activator	HGMS	Anther dehiscence, transcriptional regulation	[120]
	MYB33 MYB65	At5g06100 At3g11440	R2R3 MYB transcription factor	TGMS	Tapetum PCD, transcriptional regulation	[62]
	CER1	At1g02205	Acyl-CoA synthetase	HGMS	Pollen coat function	[82]
	CER3	At5g57800	Acyl-CoA synthetase	HGMS	Pollen coat function	[84]
	CER6/CUT1	At1g68530	Acyl-CoA synthetase	HGMS	Pollen coat function	[89]
	CER8, LACS4	At2g47240, At4g23850	Acyl-CoA synthetase	HGMS	Pollen coat function	[90]
	FKP	At4g11820	3-hydroxy-3-methylglutaryl-coenzyme A Synthase	HGMS	Pollen coat function	[121]
Rice	UGP1	Os09g0553200	UDP-glucose pyrophosphorylase1	TGMS	RNA processing	[27]
	TMS5	Os02g0214300	RNase ZS1	TGMS	RNA processing	[22]
	TMS10 -TMS10L	Os02g0283800-LOC_Os03g49620	LRR-RLK	TGMS	Signaling transduction	[19]
	TMS9-1/OSMS1	Os09g0449000	PHD finger protein	TGMS	Protein location and transcriptional regulation	[63]
	AGO1d	Os06g0729300	Argonaute protein	TGMS	PhasiRNAs production	[53,54]
	HMS1-HMS1I	Os03g0220100-Os01g0150000	3-ketoacyl-CoA synthase 6 very-long-chain enoyl-CoA reductase	HGMS	Pollen coat function	[32]
	OSOSC12 /OSPTS1	Os08g0223900	Bicyclic triterpene synthase	HGMS	Pollen coat function	[81]
	OsCER1/ OsGL1-4	Os02g0621300	Acyl-CoA synthetase	HGMS	Pollen coat function	[91]
	CSA	Os01g0274800	R2R3 MYB transcription factor	rPGMS	Sugar distribution, transcriptional regulation	[23,24]
	CSA2	Os05g049060	R2R3 MYB transcription factor	PGMS	Sugar distribution, transcriptional regulation	[26]
	PMS1	AK242308	lncRNA	PGMS	lncRNA regulation	[29]
	P/TMS12-1 (PMS3)	Os12g0545900	lncRNA, smR5864	P/TGMS	lncRNA regulation and smRNA regulation	[51,52]
	OsPDCD5	AY327105	Programmed cell death 5 protein	PGMS	Tapetum PCD	[122]
	OSMYOXIB	Os02g0816900	Myosin XI B	PGMS	Nutrition transport, protein location	[123]
	OsNP1/OsTMS18	Os10g0524500	Glucose–methanol–choline oxidoreductase	TGMS	Pollen exine formation	[97]
	ORMDL/tms2	Os07g0452500	Orosomucoid	TGMS	Sphingolipid homeostasis,PCD	[124]
	OsOAT	LOC_Os03g44150	Ornithine δ-aminotransferase	rTGMS	Cold tolerance	[125]
	HSP60-3B	LOC_Os10g32550	Heat Shock Protein60-3B	TGMS	Starch granule biogenesis, reactive oxygen species (ROS) levels	[126]
	OsTMS15	LOC_Os01g68870	LRR-RLK	TGMS	Tapetum development	[44]
	OsAL5	LOC_Os05g34640	Alfin like	TGMS	TMS5 expression	[60]
Maize	TMS5	LOC100285786	RNase ZS1	TGMS	mRNA decay	[127]
Maize	DCL5	LOC103643440	Dicer-like 5	TGMS	PhasiRNAs production	[56]
	MAGO1, MAGO2	Zm00001d007786, Zm00001d013063	MALE-ASSOCIATED ARGONAUTE	TGMS	Pre-meiotic phasiRNA pathways	[55]
	INVAN6	Zm00001d015094	Alkaline/neutral invertase	TGMS	Sugar accumulation, metabolism, and signaling	[128]
Brassica napus	BnChimera	BnRf^b	naA7.mtHSP70-1-like	rTGMS	Fatty acid synthesis	[99]
Barley	HvMS1	LOC123121697	PHD finger protein	rTGMS	Transcriptional regulation	[129]
Soybean	MS3	GLYMA_02G107600	PHD finger protein	rPGMS	Transcriptional regulation	[64]
EGMS, environment-sensitive genic male sterility; PGMS, photoperiod-sensitive genic male sterility; rPGMS, reverse photoperiod-sensitive genic male sterility; TGMS, thermo-sensitive genic male sterility; rTGMS, reverse thermo-sensitive genic male sterility; HGMS, humidity-sensitive genic male sterility.

Table 1.

Genes involved in environmental adaption of plant male reproduction.