Functional genomics and signaling events in mycorrhizal symbiosis

Figures & data

Figure 1. Chemical structure of strigolactones and their derivatives. The related strigolactone precursor and their derivative compounds involved in arbuscular mycorrhizal symbiosis signaling event. The compound 5-deoxystrigol is considered as the common precursor of strigolactone and its derivatives.

Figure 2. Biosynthetic pathway of strigolactone biosynthesis. Biosynthesis of strigolactone and its related molecules involved in mycorrhizal symbiosis signaling event starts from the carotenoid molecule of plant. Different genes involved in this process are indicated in figure. Study shows that loss of function mutant of different genes involved in biosynthetic process fails to synthesize SL molecule properly and resulted in abnormal/altered or no mycorrhizal symbiosis.

Figure 3. Figure representing perception of arbuscular mycorrhizal Nod/Myc factor by the respective receptor molecule. Upon perception of Nod/Myc signal, receptor molecule passed the signal to downsteam part which in turn activates the second messengers in cytoplasm. The second messengers led to activation of CASTOR, POLLUX or DMI1 like molecules. Upon activation of CASTOR, POLLUX, or DMI1 molecule, K⁺ ion released out from nucleoplasm making the cytoplasm hyperpolarized. Once the cytoplasm gets hyperpolarized, perinuclear Ca²⁺ ion enters into the nucleoplasm resulting in Ca²⁺ spiking. The Ca²⁺ ion binds to CCaMK which in turn passes the signal to CYCLOPOS gene responsible for regulation of mycorrhization process.

Table 1. Table showing list of genes and their roles during mycorrhizal symbiosis process.

Symbiotic Genes	Gene product	Function	Phenotype	References
Genes involved in strigolactone biosynthesis and signaling
CCD7	Carotenoid cleavage dioxygenase	Strigolactone synthesis	Reduced colonization	(Gomez-Roldan et al. 2008)
CCD8	Carotenoid cleavage dioxygenase	Strigolactone synthesis	Reduced colonization	(Gomez-Roldan et al. 2008)
D27	Carotenoid isomerase	Strigolactone synthesis	Not tested	(Alder et al. 2012)
PDR1	ABC Transporter	Strigolactone transport	Reduced colonization	(Kretzschmar et al. 2012)
NCED	9-cis-epoxycarotenoid cleavage dioxygenase	Strigolactone synthesis	Not studied	(López-Ráez et al. 2010)
D14/DAD2/HTD2	β-hydrolase family receptor	Perceive strigolactone signaling	Not studied	(Zhou et al. 2013)
DWARF53 (D53)	class I Clp ATPase	Repressor of strigolactone synthesis	Insensitive to strigolactone signaling	(Zhou et al. 2013)
DWARF3 (D3)	F-box protein	Strigolactone response	Defects in fungal colonization	(Yoshida et al. 2012)
DWARF14	Hydrolase family protein	Strigolactone response	Higher AM fungal colonization	(Yoshida et al. 2012)
Genes involved in symbiotic events
GINI	Hedghog protein	Germination of fungal spore	Not studied	(Requena et al. 2002)
EARLY NODULINE ENOD12	Serine protease	Signal transduction in SYM8 pathway	Not studied	(Albrecht & Lapeyrie 1998)
DMI2	Receptor like kinase	Myc-LCOs signaling	Reduced colonization	(Maillet et al. 2011)
LNP	Lectin nucleotide phosphohydrolase	Nod factor binding protein	Nodulation	(Roberts et al. 2013)
NUP85	Nucleoporin	Nuclear trafficking	Reduced colonization	(Kanamori et al. 2006)
NUP133	Nucleoporin	Nuclear trafficking	Reduced colonization	(Saito et al. 2007)
NENA	Nucleoporin	Nuclear trafficking	Reduced colonization	(Groth et al. 2010)
NSP2	GRAS transcription factor	Transcription factor	Reduced colonization	(Maillet et al. 2011)
RAM1	GRAS transcription factor	Transcription factor	No hypopodium	(Wang et al. 2012)
RAM2	GPAT	Cutin monomer biosynthesis	No hypopodium	(Gobbato et al. 2012)
VAPYRIN	MSP and ANK repeat containing protein	Unknown	No arbuscules	(Pumplin et al. 2010)
VAMP72	Exocytotic vesicle associated membrane protein	Formation of periarbuscular membrane	Stunted arbuscules	(Ivanov et al. 2012)
SbtM1	Subtilisin-like protease	Unknown	Reduced colonization and reduced arbuscules	(Takeda et al. 2009)
SbtM3	Subtilisin-like protease	Unknown	Reduced colonization and reduced arbuscules	(Takeda et al. 2009)
STR1	Half ABC transporter	Unknown	Reduced colonization and stunted arbuscules	(Gutjahr et al. 2012)
STR2	Half ABC transporter	Unknown	Reduced colonization and stunted arbuscules	(Gutjahr et al. 2012)
DELLA	DELLA	Transcriptional Regulator	Arbuscle formation	(Floss et al. 2013)
Genes involved in calcium signaling
DMI1	Cation channel	Calcium spiking PPA formation	Reduced colonization Fails to assemble PPA	(Ané et al. 2004) (Genre et al. 2005)
DMI3	Calcium/calmodulin dependent protein kinase	Calcium spiking	No colonization	(Catoira et al. 2000; Capoen et al. 2011)
IPD3	Coiled-coil domain containing protein	Interacts with DMI3	No arbuscules	(Horváth et al. 2011)
MCA8	Calcium pump	Calcium spiking	Reduced colonization	(Capoen et al. 2011)
CASTOR, POLLUX, and CYCLOPOS	Ion channel	Calcium spiking	Impaired in calcium spiking	(Charpentier et al. 2008)
	Coiled coil motif with nuclear localization signal	Interacts with CCaMK in nucleus	Impaired in AM colonization	(Yano et al. 2008; Singh et al. 2014)
Genes involved in nutrient uptake
PT4	Phosphate transporter	Symbiotic phosphate uptake	Reduced symbiotic phosphate uptake	(Javot et al. 2007)
PT10	Phosphate transporter	Symbiotic phosphate uptake	Not studied	(Tamura et al. 2014)
PT11	Phosphate transporter	Symbiotic phosphate uptake	Reduced symbiotic phosphate uptake	(Paszkowski et al. 2002)
AMT2	Nitrate transporter	Symbiotic nitrate uptake	Not studied	(Guether et al. 2009)
Genes involved in hormonal regulation
DGT	Cyclophilin	Gravitropism and lateral root formation	Lack presymbiotic root branching
PCT	Negative regulator of polar auxin transport	Cotyledon formation	Stimulated presymbiotic root branching	(Hanlon & Coenen 2011)
BSH	SNF5 type protein	Auxin signaling	Reduced mycorrhizal colonization	(Foo 2013)
DELLA	Della protein	Gibberellin signaling	Reduced mycorrhizal colonization	(Foo, Ross, et al. 2013)
SPR2	Fatty acid desaturase	Biosynthesis of jasmonic acid	Reduced mycorrhizal colonization	(Li et al. 2002)
miRNA in mycorrhizal symbiosis
miR5229a/b	microRNA5229a/b	Targets Haem-Peroxidase	Arbuscules development	(Branscheid et al. 2011)
miR171h	microRNA171h	Targets NSP2	Increase root colonization and arbuscules formation	(Lauressergues et al. 2012)
miR169	microRNA169	Targets BCP1	Arbuscules development	(Pumplin & Harrison 2009)
miR5204	microRNA5204	Targets GRAS transcription factor	Decrease in mycorrhizal colonization via GRAS cleavage	(Gobbato et al. 2012)
miR160f	microRNA160f	Targets auxin response factor gene family	AM symbiosis	(Branscheid et al. 2011)
miR160c	microRNA60c	Targets auxin response factor gene family	AM symbiosis	(Branscheid et al. 2011)
miR5282	microRNA5282	Targets Glutathione s-transferase	Involved in ROS mediated mycorrhization	(Wulf et al. 2003b)
miR399	microRNA399	Targets PHO2 phosphate transporter	Involved in cellular phosphate homeostasis	(Branscheid et al. 2010)
miR159b	microRNA159b	Targets Erf transcription factor	Targeted silencing led to deformed arbuscules	(Devers et al. 2013)

Figure 4. Figure depicting soil, mycorrhiza and plant interfaces involved in nutrient uptake during mycorrhizal symbiosis process. The fungi receive different nutrient supplement from soil and transports them to its symbiotic plant partner. Nutrient transfer from soil by mycorrhizal fungus occurred via different transporter molecules. Different transporter molecules involved in this process are phosphate, amino acids, urea, ammonia and nitrate transporters. Similarly, fungus receives its carbon source like fructose, sucrose etc. from host plant via specialized transporter molecule in exchange of nutrient supply.

Figure 5. The calcium spiking events by DMI1, POLLUX and CASTOR genes during arbuscular mycorrhizal symbiosis as proposed by Venkateshwaran et al. (2012). They proposed that an unknown secondary messenger activates cation channels like DMI1 or CASTOR-POLLUX. The CASTOR and POLLUX responsible for permeation of K⁺ ion in favor of their concentration gradient from cytoplasm to perinuclear space. The permeation of K⁺ by DMI1, CASTOR and POLLUX lead to hyperpolarization of nuclear membrane. Upon hyperpolarization, hyperpolarized mediated gated Ca²⁺ channels get activated. This leds to flow of perinuclear Ca²⁺ ions to cytoplasm and nucleoplasm giving rise to Ca²⁺ spike and calcium mediated signaling. As Ca²⁺ enters into cytoplasm and nucleoplasm, it reduces the hyperpolarization of cytoplasm. This led to closure of hyperpolarization mediated Ca²⁺ channels. Once calcium mediated signaling is over, Ca²⁺ ions pumped out from cell by Ca²⁺ mediated ATPase, MCA8 resulting in resting potential of cell. Figure prepared as hypothesized by Venkateshwaran et al. (2012).

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