Figures (2)  Tables (3)

    • Figure 1.  A proposed schematic diagram of endophyte-infected and endophyte-free plant responses to increasing soil water deficit. Figure adapted from Assuero et al.[63].

    • Figure 2.  Three-year-old perennial ryegrass trial in the Waikato, New Zealand. Plants in plots that have not survived were either endophyte-free or infected with an endophyte strain that did not protect the host plant against Argentine stem weevil or African black beetle during dry summers.

    • InsectAdult and larvae Argentine stem weevil (Listronotus bonariensis)Pasture mealybug (Balanococcus poae)African black beetle (Heteronychus arator)Root aphid (Aploneura
      lentisci)      		Porina (Wiseana spp.)Grass grub (Costelytra zealandica)Black field cricket (Teleogryllus commodus)Animal health disorders
      Annual economic impact in a specific industry[20]Up to $\$ $200M dairy; $\$ $235M sheep & beefUnknownUp to $\$ $223M dairy; $\$ $19M sheep & beefUnknownUp to $\$ $84M dairy; $\$ $88M sheep & beef$\$ $275M−$\$ $706M dairy; $\$ $75M−$\$ $205M sheep & beefUnknown
      Diploid perennial ryegrass (E. festucae var. lolii)
      AR1Peramine++++[21]++++[22]+[23]−2[24]−[25]−[26]not testednone[10]
      AR37Epoxy-janthitrems++++1[27]++++[22]+++[28]++++[24]+++[25]+[26]not testedoccasionally[29,30]
      NEA2Peramine, ergovaline, lolitrem B+++[26](++++)[26]+++[26]++[24]not tested−[26]not testednone[26]
      NEA4Peramine, ergovaline+++[26](++++)[26]+++[26]++[26]not testednot testednot testednone[26]
      EdgePeramine, ergovaline(++++)*(++++)*(+++)*(+++)*(−)*not testednot testednone*
      Avanex®Peramine, ergovaline, lolitrem B########
      Diploid perennial ryegrass (E. siegelii)
      HappeLolines(+++)*(++++)*(+++)*(++++)*(++++)*not testednot testednot tested
      Tetraploid perennial ryegrass (E. festucae var. lolii)
      AR1Peramine(+++)[26](++++)[26]+[26]−2[26]−[26]−not testednone
      AR37Epoxy-janthitrems(+++)1[26](++++)[26]+++[26]++++[26](+++)[26]+not testedoccasionally[29,30]
      Italian and hybrid ryegrass (E. festucae var. lolii)
      AR1Peramine++[26](++++)[26]+[26]−[26]not tested−not testednone
      NEAPeramine, ergovaline, lolitrem BNot tested(++++)[26]+++[26]not testednot tested−not testednone
      AR37Epoxy-janthitrems+++1[26](++++)[26]+++[26]not testednot tested−not testedoccasionally[29,30]
      Festulolium (E. uncinata)
      U2Lolines++++[31](++++)[32]++++3[26]++++[26](++)[26]+++[33]+++[26]none
      Meadow fescue (E. uncinata)4
      Tall fescue (E. coenophiala)
      MaxP/MaxQPeramine, lolines(++++)[34](++++)[32]++++[26](++++)[26](++T)[35]+++R[35]++++[36]none[36]
      ProtekLolines(++++)*(++++)*(++++)*(++++)*(++++)*(++++)*(++++)*none*
      − No protection.
      + Low level of control: Endophyte may provide a measurable effect, but is unlikely to give control in the field;
      ++ Moderate level of control: Endophyte may provide some protection in the field, with a low to moderate reduction of pest population.
      +++ Good level of control: Endophyte significantly reduces insect damage under low to moderate insect pressure. Damage might occur during high insect pressure
      ++++ Very good control: Endophyte significantly reduces insect damage and pest population even under high pest pressure.
      () Provisional rating: Testing is ongoing, further data is required to support rating.
      1 AR37 only deters the more damaging ASW larvae not adult.
      2 AR1 plants are more harmed than plants without endophyte.
      3 Active against Black beetle adult and larvae.
      4 A new meadow fescue cultivar infected with E. uncinata is now commercially available but has yet to be formally rated for its effects on insect pests. Previous work has shown that natural meadow fescue endophytes provide strong protection against a range of insect pests including black beetle, Argentine stem weevil and crickets[37−39]
      * DLF Seeds & Science; ratings have not been approved by the New Zealand Plant Breeding & Research Association.
      T - Higher plant growth compared with endophyte-free control but no difference in larval weight.
      R - Reduced weight gain of grass grub larvae.
      # - Toxic endophyte used at airports and sports fields to reduce the number of birds on or near sports fields and airfields[40].

      Table 1.  Summary of Epichloë endophyte brands in ryegrass and fescue grasses available in New Zealand, Australia, and the USA: alkaloid profile, insect resistance properties, and livestock toxicity for each.

    • Species of grass and
      endophyte      		Impact of endophytePhysiological and/or structural changes to host plant and endophyte in response to droughtReference
      Cultivated grasses
      Perennial ryegrass
      (L. perenne)
      E. festucae var. lolii      		Increased tiller number and shoot weight15% higher osmotic potential[64]
      Leaf water content not affected[65]
      Reduced leaf dehydration in moderately droughted plants[66]
      Variable effect related to original habitat of collectionIncreased root dry weight and root/shoot ratio[67]
      Lower dry weight, but less wiltingLower water use efficiency[68]
      In 4 of 6 Mediterranean populations endophyte improved drought toleranceIncreased tiller number and yield[69]
      Beneficial for combined stresses of drought and Bipolaris sorokinianaIncreased growth, and photosynthetic parameter, but decreased proline content[70]
      Provides physiological protection against droughtDrought increased ergovaline and lolitrem B levels but endophyte had no effect on proline levels improved water use efficiency, relative water content and osmotic potential[71]
      No effectNo effect on osmotic potential[72]
      No effect on stomatal conductance[62,73,74]
      No involvement to withstand or recover from drought[75−78]
      Higher seedling survival when released from droughtNo effect on reactive oxygen species[79]
      Tall fescue
      (F. arundinacea)
      E. coenophiala      		Endophyte responses vary with genotypePseudostem, root and dead leaf yield increased with endophyte in some cases; no effect on non-structural carbohydrates[80]
      No consistent endophyte effect on dry weight per tiller, stomatal conductance; endophyte reduced leaf rolling in drought, but increased water content and delayed desiccation[81]
      No effect on leaf osmotic potential and minimal effect on plant water-soluble mineral and sugar concentrations[82]
      Improved plant survival under severe soil moisture deficitLeaf rolling under drought stress greater for endophytic plants; regrowth greater for endophytic plants when re-watered[83]
      Increased alkaloid levels[80,84,85]
      Increased soluble carbohydrates in leaves[63,86,87]
      Shedding of older leaves and rolling of younger leaves; low stomatal conductance; increased cellular turgor pressure[63,88]
      No effect on leaf rolling[89]
      Enhanced tiller density and plant survival[90]
      Maintained water use efficiency and photosynthetic rate better under drought[91]
      Enhanced osmotic adjustment in meristem; reduced stomatal conductance and transpiration[92,93]
      Reduced stomatal conductance; maintained higher water content of tiller bases[93]
      Root nematode inhibition by endophyte enhances drought tolerance[90,94]
      Increased plant available water[95]
      Reduced reactive oxygen species[96]
      Improved recovery after droughtImproved tiller and whole plant survival[62,87,90,97−99]
      Improved root growth[100]
      Meadow fescue
      (F. pratensis)
      E. uncinatum      		Improved growth in droughtReduced stomatal conductance[101,102]
      Increased water uptake capacity[103]
      Production of larger but fewer tillers[104]
      Strong creeping red fescue
      (F. rubra ssp. rubra) –
      turf type E. festucae      		No improvement under drought[105]
      Native grasses
      Drunken horse grass
      (Achnatherum inebrians)
      E. gansuense      		Improved tolerance to drought and recovery from droughtIncreased leaf proline, root/leaf growth, tiller number[106]
      Improved photosynthetic efficiency and nutrient absorption[107]
      Increased ergovaline and ergine alkaloid concentrations[108]
      Reduced disease incidence of Blumeria graminis[109]
      Achnatherum sibiricum
      Epichloë spp.      		Endophyte benefit greatest when well-watered and fertilisedHigher root: shoot ratio and photosynthetic rate under drought and fertiliation[110]
      Hordelymus europaeus
      E. hordelymi      		Improved recovery from droughtIncreased tiller number and plant dry weight[111]
      Grove bluegrass
      (Poa alsodes)
      Epichloë spp.      		Improved the negative effects of drought stressEndophytic plants under drought had 24% more root biomass, 14% more shoot biomass; 29% more leaf senescence in non-endophytic plants[112]
      Arizona fescue
      (Festuca arizonica)
      Epichloë spp.      		Endophyte infection beneficial in droughtIncreased growth rates; low net photosynthesis and stomatal conductance[113]
      Bromus auleticus
      E. pampeanum and
      E. tembladerae      		Improved survival in summerHigher regrowth rate[114]
      Roegneria kamoji
      E. sinica      		Improved seedling establishment in droughtImproved germination and seedling growth[115]
      Elymus dahuricus
      Epichloë spp.      		Improved yield and tiller numbers under droughtEndophyte caused anti-oxidative enzyme activities and contents of proline and chlorophyll a + b increased under drought[116]
      Increased germination at moderate osmotic potentials[117]
      Elymus virginicus
      E. elymi      		Improved drought tolerance, but also benefited well-watered plantsNo effect on root: shoot ratio; improved tiller number[118]
      Leymus chinensis
      E. bromicola      		Improved yield under droughtIncreased photosynthetic rate[119]
      Festuca sinensis
      Epichloë spp.      		Endophytes enhanced drought toleranceIncreased yield, root: shoot ratio[120]

      Table 2.  The impact of Epichloë endophyte on the drought tolerance of a range of cultivated and native temperate grasses.

    • Endophyte type and trial protocolKnown alkaloid expressionInsect pestDrought effectReference
      Ryegrass
      Italian ryegrass
      (L. multiflorum)
      E. occultans (presumably)
      Pot trial in a glasshouse      		Lolines and peramineGrass aphid
      (Sipha maydis)
      Cherry-oat aphid (Rhopalosiphum padi)      		Endophyte reduced aphid numbers but only on drought stressed plants. Aphid herbivory detrimental to endophyte infected well-watered plants.
      Interactions between drought and aphids affected reproductive tillering in endophyte-free plants only.      		[138]
      Perennial ryegrass
      (L. perenne)
      E. festucae var. lolii
      Field trial; visual assessment of larval damage scored      		Dependent on endophyte strain: ergovaline, peramine, lolitrem BBlack beetle (Heteronychus arator)Summer/early autumn drought plus differences in black beetle root damage decreased plant survival and growth of susceptible plant-endophyte combinations compared with a resistant one.[139]
      Perennial ryegrass
      (L. perenne)
      E. festucae var. lolii
      Field trial      		Dependent on endophyte strain: ergovaline, peramine, lolitrem B, epoxy-janthiremsRoot aphid (Aploneura lentisci)
      Field measurements of population densities and ryegrass growth      		Drought may have increased aphid populations and likely exacerbated their effect on plant growth. Two endophytes strongly reduced populations. Aphid populations correlated with plant growth.[140]
      Fescue
      Tall fescue
      (F. arundinacea)
      E. coenophiala
      Pot trial in a glasshouse      		N-acetyl and N-formyl lolinesNumber of cherry-oat aphids (Rhopalosiphum padi)Aphid density reduced by endophyte, and by drought stress in endophyte-free plants only.[141]
      Development time of fall armyworm (Spodoptera frugiperda)Growth and development reduced by endophyte-infected drought stressed herbage compared with well-watered. No effect on larvae fed Nil herbage.[141]
      Growth of fall armyworm (Spodoptera frugiperda)
      Tall fescue
      (F. arundinacea)
      E. coenophiala
      AR584
      Excised roots from treated plants feed to 3rd instar grass grub      		LolinesGrass grub (Costelytra given) 3rd instar larvaeRoot consumption of endophyte-free plants higher if plants droughted compared with well-watered endophyte-free; larval weight change reduced by endophyte fed droughted plant roots. Loline concentration in roots higher in droughted than in well-watered plants.[142]
      Meadow fescue (F. pratensis)
      E. uncinata
      Excised roots fed to 3rd instar grass grub      		Endophyte reduced root consumption, frass output, and larval weight change; effects greatest for well-watered plants; loline concentration higher in roots of well-watered plants than droughted plants.[142]
      Red fescue
      (F. rubra)
      E. festucae
      Field survey and common garden experiment      		ErgovalineLocusts
      Locusta migratoria)      		Endophyte significantly reduced weight and survival of locusts[143],
      [144]

      Table 3.  Impact of Epichloë on the interaction between drought and insect herbivory