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Insights into Plant-Microbial
Symbiosis and Implications for
Sustainable Agriculture –
Giving Attention to ‘Inner Space’
Norman Uphoff, SRI-Rice, Cornell University
National Institute for Agricultural and
Forestry Research (IDIAP),
Santo Domingo, January 26, 2013
A challenge for our 21st century agriculture
is to produce MORE with LESS
Necessary to achieve sustainable development
• This may sound impossible or improbable
• However, it may be achieved by working more
successfully within the realm of BIOLOGY,
which operates differently from the realms of
chemistry and engineering – can be ‘win-win’
Transformation of inputs into outputs is a
generic process; however, BIOLOGY
operates within open systems with options
for mobilizing energy and nutrients that
are otherwise unutilized or underutilized
In the 21st century agriculture,
we cannot just do ‘more of the same’
• Arable land area per capita is reducing as
• Populations continue to grow, while
• Land area is being lost to urban spread, and
• Land degradation is increasing year by year
• Water supply for agriculture is declining
• Competing demands for domestic use and industry
• Climate change is reducing amount and reliability
• Pests and diseases are likely to increase
In the US, crop losses to insects rose from 7% to 13%,
while the use of insecticides was increased by 14x
• Future energy prices will be higher in this
centure than in the 20th century, affecting:
• Production costs: fuel, fertilizer, agrochemicals
• Transport cost: long-distance trade more costly
• Climate patterns will become less favorable
• Impact will be greatest in poorest countries
• Accessibility of technology remains big issue
• The Green Revolution by-passed most of the
world’s poor ; must enable them to meet needs
• Scale-neutral technologies are most desirable
• Agric. productivity gains have slowed down
GREEN REVOLUTION TECHNOLOGY
was based on two main factors:
A. Improvements in GENETIC POTENTIALS,
i.e., in crop and animal genotypes (varieties)
B. Increasing application of EXTERNAL INPUTS
-- inorganic fertilizers, biocides, etc.
These elements were successful in the past, but:
• Economic costs of production are increasing,
• Environmental costs are increasing, and now
• Diminishing returns are evident, e.g., in China,
the ratio of additional rice production from 1 kg
of N has fallen from 20:1 to 5:1, and still declining
Where do we go from here?
More of the same,
but better?
Green Revolution was shaped more by
chemistry, engineering and genetics
than by biology (physiology and
microbiology) and by ecology
It ignored the contributions made by
plant roots and by the soil biota
Our challenge for sustainable agriculture is to
produce MORE OUTPUT with REDUCED INPUTS
learning how to get more productive PHENOTYPES
from available GENOTYPES – can be done by making
beneficial changes in crops’ growing environments
The System of Rice Intensification (SRI) developed
in Madagascar has shown how farmers can get
more productive rice plants from existing varieties
(local, HYVs, hybrids) at same time giving crops
more resistance to effects of CLIMATE-CHANGE:
• More DROUGHT resistance
• Resistance to STORM DAMAGE (less lodging)
• More resistance to PEST & DISEASE HAZARDS
• Even some tolerance of temperature extremes
Its methods are being adapted to many OTHER CROPS
The Basic Ideas for SRI/SCI:
• Establish healthy plants early (young) and carefully,
making efforts to maintain their root growth potential.
• Reduce plant density, giving each plant more room to
grow, both above-ground and below-ground, to capture
more sunlight and obtain more soil nutrients.
• Keep the soil well-aerated and enriched with organic
nutrients, as much as possible, so that it can support
better growth of roots and more aerobic soil biota.
– Apply water in ways that can best support the growth of
plant roots and of beneficial soil microbes, avoiding
continuous inundation and anaerobic soil conditions.
– Control weeds in soil-aerating way (mechanical weeder).
When used together, these practices enable farmers to:
(a) increase the size and functioning of ROOT SYSTEMS,
and (b) enhance the populations of beneficial SOIL BIOTA.
Farmer with
a rice plant
grown from
a single
seed with
SRI methods
in Morang
district of
NEPAL
Farmer with two plants of same variety
(VN 2084) and same age (52 DAS) in CUBA
Comparison trials at Al-Mishkhab Rice Research Station, Najaf, in IRAQ
SRI
0
50
100
150
200
250
300
IH H FH MR WR YRStage
Organdryweight(g/hill)
IH H FH MR WR YR
CK Yellow leaf
and sheath
Panicle
Leaf
Sheath
Stem
47.9% 34.7%
Non-Flooding Rice Farming Technology in Irrigated Paddy Field
Dr. Tao Longxing, China National Rice Research Institute, 2004
SRI methods have set a new world record
Paddy production: Bihar
panchayat breaks China’s record
New Delhi, Mar 20:
A gram panchayat in Nalanda district of Bihar has
surpassed the Chinese record of paddy production,
the Union Agriculture Minister Mr Sharad Pawar
informed Parliament today. “As per the reports
received from the state government, the yield of wet
paddy has been recorded at 22.4 tonnes per hectare
and that of dry paddy at 20.16 tonnes a hectare ...,”
Mr Pawar said in a written reply to Lok Sabha.
The record yield was achieved under demonstration
on System of Rice Intensification (SRI) which was
organised at farmer’s field during kharif 2011, he
added. “It has surpassed the yield of 19 tonnes per
hectare which was recorded earlier in China.”
Before 1999: Madagascar
1999-2000: China, Indonesia
2001-02: Bangladesh, Cuba, Laos,
Cambodia, Gambia, India, Nepal,
Myanmar, Philippines, Sierra Leone,
Sri Lanka, Thailand
2003: Benin, Guinea, Mozambique, Peru
2004-05: Senegal, Pakistan, Vietnam
2006: Burkina Faso, Bhutan, Iran, Iraq,
Zambia
2007: Afghanistan, Brazil, Mali
2008: Rwanda, Costa Rica, Egypt,
Ecuador, Ghana, Japan
2009: Malaysia, Timor Leste
2010: Kenya, DPRK, Panama, Haiti
2011: Colombia, Korea, Taiwan,
Tanzania
2012: Burundi, Dominican Republic,
Niger, Nigeria, Togo (total of 51)
2012: >50 countries of Asia, Africa, and Latin America
where SRI’s phenotypic benefits have been seen
Agroecological methods can give
significant increases in yield,
by multiples rather than increments,
for resource-limited households
with reduced inputs (seeds, water, fertilizer)
* ‘Intensification’ is of farmer’s knowledge,
skill and management -- rather than of
purchased inputs – but also, with
mechanization it is possible to save labor
* Changes are made in the management of
plants, soil, water and nutrients to affect
the populations and activity of soil biota
INDONESIA
Caritas introduced
SRI methods in Aceh
in 2005 after tsunami
devastation – local
rice yields were
raised from 2 t/ha to
8.5 t/ha
“Using less rice seed, less water and organic compost,
farmers in Aceh have quadrupled their crop production.”
‘Rice Aplenty in Aceh,’ Caritas News (2009)
Similar quadrupling of yield by poor, food-insecure, resource-
limited households has been documented also in Madagascar,
Cambodia, and Madhya Pradesh (India)
INDIA:
Report in
The HINDU
Nov. 28, 2011
on SRI results in
Madhya Pradesh
SRI methods were introduced in Damoh district of
Madhya Pradesh state by Gramin Vikas Samiti,
with support from the People’s Science Institute (PSI)
More than 1,200 farmers in 32 villages increased their average
paddy yields from 1.7-2.0 t/ha to 7.5-8.0 t/ha
with minimum of 4.4 t/ha and maximum of 11.5 t/ha
-- using traditional varieties and with organic management
SRI panicle with traditional variety (top);
HYV panicle with usual mgmt (bottom)
Hang Hein’s field was transplanted in one day by his 3 sons below;
traditional transplanting methods are shown on right; with SRI crop
management, Hang Hein’s yield went from 1.25 t/ha to 5 t/ha
CAMBODIA: SRI introduced in Kampong Chhnang province
in 2006-2007 by LDS Charities, with 146 farmers whose
rainfed yields had previously averaged just 1.06 t/ha --
their yields with SRI practices averaged 4.02 t/ha
These changes in crop management
are effective in very different and
quite contrasting agroecosystems:
* AFGHANISTAN: Baghlan province
1600 masl, temperate climate;
short growing season
* MALI: Timbuktu province
on edge of Sahara Desert;
hot, dry tropical climate
AFGHANISTAN: SRI field in Baghlan Province, supported by
Aga Khan Foundation Natural Resource Management program
AKF technician making a field visit in Baghlan province
SRI field at 30 days
SRI plant with
133 tillers @
72 days after
transplanting 11.56 t/ha
* Some areas could not continue or
be measured because of Taliban
SRI yields were achieved
with reductions in water
Year
SRI
Users
SRI
Yield
Conv.
Yield
2008 6 10.1 5.4
2009 42 9.3 5.6
2nd yr [7] [13.3] [5.6]
1st yr [35] [8.7] [5.5]
2010 104 8.8 5.6
2011 114* 10.01 5.04
MALI -- SRI nursery in Timbuktu region –
8-day seedlings ready for transplanting
SRI transplanting on
edge of Sahara Desert
Malian farmer in the
Timbuktu region
showing the difference
between regular and
SRI rice plants
with 32% less water
Gao region: 7.84 t/ha
Mopti region: 7.85 t/ha
Year
SRI
Users
SRI
Yield
Conv.
Yield
2007-08 1 8.98 --
2008-09 60 9.01 5.49
2009-10 130 7.71 4.48
Environmental Benefits with SRI:
1. Reduced water requirements – higher crop water-use
efficiency -- puts less pressure on ecosystems in
competition with agriculture for water supplies
2. Higher land productivity – reducingpressures for the
expansion of arable area to feed our populations
3. Less use of inorganic fertilizer – reactive N is “the third
major threat to our planet after biodiversity loss and
climate change” (John Lawton, former chief executive,
UK National Environmental Research Council)
4. Less reliance on agrochemicals for crop protection -
which enhances the quality of both soil and water
5. Buffering the effects of climate change – drought,
storms (resist lodging), cold temperatures, etc.
6. Possible reduction in greenhouse gases (GHG) – CH4 is
reduced apparently without producing offsetting N2O
Other Benefits from Changes in Practices
1. Water saving – major concern in many places, also
now have ‘rainfed’ version with similar results
2. Greater resistance to biotic and abiotic stresses –
less damage from pests and diseases, drought,
typhoons, flooding, cold spells [discuss tomorrow]
3. Shorter crop cycle – same varieties are harvested
by 1-3 weeks sooner, save water, less crop risk
4. High milling output – by about 15%, due to fewer
unfilled grains (less chaff) and fewer broken grains
5. Reductions in labor requirements – widely reported
incentive for changing practices in India and China;
also, mechanization is being introduced many places
6. Reductions in costs of production – greater farmer
income and profitability, also health benefits
Drought-resistance: Rice fields in Sri Lanka, same variety
and same soil 3 weeks after irrigation had stopped because
of drought – conventional rice field (left) and SRI (right)
INDIA: Results from Bihar State, 2007-2012
SYSTEM OF RICE INTENSIFICATION -- state average yield: 2.3 t/ha
2007 2008 2009 2010 2012
Climatic conditions
Normal
rainfall
2x
flooding
Drought +
rain in Sept.
Complete
drought
Good
rainfall
No. of smallholders 128 5,146 8,367 19,911 NR
Area under SRI (ha) 30 544 786 1,412 335,000
SRI yield (t/ha) 10.0 7.75 6.5 3.22* 8.08
Conv. yield (t/ha) 2.7 2.36 2.02 1.66* NR
,
SYSTEM OF WHEAT INTENSIFICATION -- state average yield: 2.4 t/ha
2007-08 2008-09 2009-10 2011-12
No. of smallholders 415 25,235 48,521 NR
Area under SWI (ha) 16 1,200 2,536 183,085
SWI yield (t/ha) 3.6 4.5 NA 5.1
Conv. yield (t/ha) 1.6 1.6 NA NR
* Results from measurements of yield on 74 farmers’ SRI and conventional fields
Year 2004 2005 2006 2007 2008 2009 2010 Total
SRI area (ha) 1,133 7,267 57,400 117,267 204,467 252,467 301,067 941,068
SRI yield (kg/ha) 9,105 9,435 8,805 9,075 9,300 9,495 9,555 9,252
Non-SRI yield (kg/ha) 7,740 7,650 7,005 7,395 7,575 7,710 7,740 7,545
SRI increment (t/ha)* 1,365 1,785 1,800# 1,680 1,725 1,785 1,815# 1,708
SRI % yield increase * 17.6% 23.3% 25.7% 22.7% 22.8% 23.2% 23.5% 22.7%
Grain increase (tons) 1,547 12,971 103,320 197,008 352,705 450,653 546,436 1.66 mill
Addl. net income from
SRI use (million RMB)* 1.28 11.64 106.5 205.1 450.8 571.7 704.3 2,051
(>$300 mill)
* Comparison with Sichuan provincial average for paddy yield and SRI returns
# Drought years: SRI yields were relatively better than with conventional methods
Source: Data are from the Sichuan Provincial Department of Agriculture.
CHINA: SRI extension/impact in Sichuan Province, 2004-10
Storm resistance:
Dông Trù village,
Ha Noi province,
Vietnam, after
fields were hit by
a tropical storm
Right: conventional
field and plant;
Left: SRI field
and plant
Same variety used
in both fields:
serious lodging
seen on right --
no lodging on left
Irrigation
method
Seedling
age
Spacing
(cm2)
Plant lodging (in percent)
Partial Complete Total
Inter-
mittent
irrigation
(AWDI)
14
30x30 6.67 0 6.67
30x18 40.00 6.67 46.67
21
30x30 26.67 20 46.67
30x18 13.33 13.33 26.67
Ordinary
irrigation
(continuous
flooding)
14
30x30 16.67 33.33 50.00
30x18 26.67 53.33 80.00
21
30x30 20 76.67 96.67
30x18 13.33 80 93.33
Lodging of rice as affected by irrigation practices
when combined with different ages of seedlings and
different spacings in trials done in Chiba, Japan
(Chapagain and Yamaji, Paddy and Water Environment, 2009)
Disease and pest resistance: Evaluation by
Vietnam National IPM Program, 2005-06 –
averages of data from on-farm trials in 8 provinces
Spring season Summer season
SRI
plots
Farmer
plots
Differ-
ence
SRI
plots
Farmer
plots
Differ-
ence
Sheath blight 6.7% 18.1% 63.0% 5.2% 19.8% 73.7%
Leaf blight -- -- -- 8.6% 36.3% 76.5%
Small leaf
folder *
63.4 107.7 41.1% 61.8 122.3 49.5%
Brown plant
hopper *
542 1,440 62.4% 545 3,214 83.0%
AVERAGE 55.5% 70.7%
* Insects/m2
Resistance to both biotic and abiotic stresses: fields in
East Java, Indonesia hit by both brown planthopper (BPH)
and by storm damage (typhoon): rice field on left was
managed with standard practices; organic SRI is seen on right
Modern
improved
variety
(Ciherang)
– no yield
Traditional
aromatic
variety
(Sintanur)
- 8 t/ha
Resistance to cold temperature: Yield and
meteorological data from ANGRAU, A.P., India
Period Mean max.
temp. 0C
Mean min.
temp. 0C
No. of sunshine
hrs
1 – 15 Nov 27.7 19.2 4.9
16–30 Nov 29.6 17.9 7.5
1 – 15 Dec 29.1 14.6 8.6
16–31 Dec 28.1 12.2# 8.6
# Sudden drop in minimum temp. for 5 days (16–21 Dec = 9.2-9.9o C )
Season Normal (t/ha) SRI (t/ha)
Kharif 2006 0.21* 4.16
Rabi 2005-06 2.25 3.47
* Low yield was due to cold injury (see below)
Comparison of methane gas emission
CT SRI
kgCH4/ha
0
200
400
600
800
1000
840.1
237.6
72 %
Treatment
Emission (kg/ha) CO2 ton/ha
equivalentCH4 N2O
CT 840.1 0 17.6
SRI 237.6 0.074 5.0
SRI practices are being used beyond RICE:
Farmer-led innovations with civil society help in:
• Wheat (SWI) -- India, Nepal, Ethiopia, Mali
• Sugarcane (SSI) -- India, Cuba
• Finger millet (SFMI) -- India, Ethiopia
• Mustard/rapeseed/canola (SMI) -- India
• Teff (STI) -- Ethiopia
• Sorghum (SSI2) – Ethiopia
• Turmeric (STI2) -- India
System of Crop Intensification (SCI): maize, black
gram, green gram, red gram, tomatoes, chillies,
eggplant, sesame, etc. -- India, Ethiopia
Wheat: SWI (left) vs. conventional plants in Bihar, India
Phenotypical
differences in
wheat panicles
with SWI practice
seen in Nepal
Tef: Application of SRI
concepts & practices
to production of tef
(STI) in Ethiopia
Left: transplanted tef
Right: broadcasted tef
3-5 t/ha vs. 1 t/ha
STI tef crop in Tigray province of Ethiopia
ICRISAT-WWF
Sugarcane Initiative:
• 20-100% more
cane yield, with
• 30% reduction in
water, and
• 25% reduction in
chemical inputs
“The inspiration for putting
this package together is
from the successful
approach of SRI – System
of Rice Intensification.”
Sugarcane: SSI cane
plants seen in India –
SSI is now getting
started in Cuba,
known as SiCAS
CUBA: SicAS sugarcane
@ 10.5 months
Eventual yield was
estimated @ 150 t/ha
Crops Yield increases
Finger millet 3-4x
Legumes 50-200%
Maize 75%
Mustard 3-4x
Sugarcane 20-100%
Tef 3-5x
Turmeric 25%
Vegetables 100-270%
Wheat 10-140%
SCI crops are mostly rainfed, but 30% water-saving
with wheat and sugarcane, 66% with turmeric
Summary of results reported from farmers' fields for
System of Crop Intensification (SCI)
applying SRI concepts and methods to other crops
These results do NOT argue against
making further genetic improvements
or against the use of external inputs
They suggest, however, that progress can be
made right now at low cost -- with saving
of water & buffering against climate change --
by changing crop management practices,
especially by attending to the purposeful
nurturing of roots and soil biota
WHAT IS GOING ON?
SRI/SCI shows us the importance of
abundance, diversity and activity of
beneficial SOIL ORGANISMS promoted
by soil organic matter and by exudates
from large, functioning ROOT SYSTEMS
that support plant growth and health
We are just starting to understand
better the contributions of symbiotic
endophytes to mobilizing the services
of plant microbiomes that aid crops
Soil-aerating hand weeder in Sri Lanka costing <$20
Effects of Active Soil Aeration
412 farmers in Morang district of Nepal
when using SRI in monsoon season, 2005
SRI yield = 6.3 t/ha vs. control yield = 3.1 t/ha
Data show how WEEDINGS can raise yield
No. of No. of Average Range
weedings farmers yield of yields
1 32 5.16 (3.6 - 7.6)
2 366 5.87 (3.5 - 11.0)
3 14 7.87 (5.85 - 10.4)
Mechanical
Weedings
Farmers
(N)
Area
(ha)
Harvest
(kg)
Yield
(t/ha)
0 2 0.11 657 5.973
1 8 0.62 3,741 7.723
2 27 3.54 26,102 7.373
3 24 5.21 47,516 9.120
4 15 5.92 69,693 11.772
Impact of weedings on yield with SRI methods
in Ambatovaky, Madagascar, 1997-98
ENDOPHYTIC AZOSPIRILLUM, TILLERING, AND RICE YIELDS
WITH CULTIVATION PRACTICES AND NUTRIENT AMENDMENTS
Replicated trials at Anjomakely, Madagascar, 2001 (Andriankaja, 2002)
CLAY SOIL Azospirillum
in roots (103
CFU/mg)
Tillers/ plant
Yield
(t/ha)
Conventional
methods, with no
soil amendments
65 17 1.8
SRI cultivation, with
no soil amendments
1,100 45 6.1
SRI cultivation,
with NPK fertilizer
450 68 9.0
SRI cultivation,
with compost
1,400 78 10.5
LOAM SOIL
SRI cultivation with
no soil amendments
75 32 2.1
SRI cultivation,
with compost
2,000 47 6.6
Microbial populations in rice rhizosphere
Tamil Nadu Agricultural University research
Microorganisms Conventional
methods
SRI
methods
Total bacteria 88 x 106 105 x 106
Azospirillum 8 x 105 31 x 105
Azotobacter 39 x 103 66 x 103
Phosphobacteria 33 x 103 59 x 103
T. M. Thiyagarajan, WRRC presentation, Tsukuba, Japan, 2004
Total bacteria Total diazotrophs
Microbial populations in rhizosphere soil in rice crop under different management
at active tillering, panicle initiation, and flowering (conv. = red; SRI = yellow).
Units are √ transformed values of population/gram of dry soil (data from IPB)
Phosphobacteria

Azotobacter
0
10
20
30
40
Dehydrogenase activity (μg TPF) Urease activity (μg NH4-N))
Microbial activities in rhizosphere soil in rice crop under different management
(conv. = red; SRI = yellow) at active tillering, panicle initiation, and flowering stages
Units are √ transformed values of population/gram of dry soil per 24 h
Acid phosphate activity (μg p-Nitrophenol)

Nitrogenase activity (nano mol C2H4)
Effects of symbiotic microorganisms
in rice plants go beyond the root zone
(the rhizosphere)
They also extend upward into the shoot
& leaves (phyllosphere) and even seeds
Contributions made by symbiotic
endophytes are just starting to be
well documented and widely known
“Ascending Migration of Endophytic Rhizobia, from
Roots and Leaves, inside Rice Plants and Assessment of
Benefits to Rice Growth Physiology”
Feng Chi et al., Applied and Envir. Microbiology 71 (2005), 7271-7278
Rhizo-
bium
strain
Total plant
root vol/pot
(cm3)
± SE
Shoot dry
wt/pot
(g)
± SE
Net photosyn-
thesis rate
(µmol of CO2
m-2 s-1) ± SE
Water
utilization
efficiency
± SE
Grain
yield/pot
(g)
± SE
Ac-ORS
571
210
± 36A
63
± 2A
16.42
± 1.39A
3.63
± 0.17BC
86
± 5A
Sm-1021 180
± 26A
67
± 5A
14.99
± 1.64B
4.02
± 0.19AB
86
± 4A
Sm-1002 168
± 8AAB
52
± 4BC
13.70
± 0.73B
4.15
± 0.32A
61
± 4B
R1-2370 175
± 23A
61
± 8AB
13.85
± 0.38B
3.36
± 0.41C
64
± 9B
Mh-93 193
± 16A
67
± 4A
13.86
± 0.76B
3.18
± 0.25CD
77
± 5A
Control 130
± 10B
47
± 6C
10.23
± 1.03C
2.77
± 0.69D
51
± 4C
“Proteomic analysis of rice seedlings infected by
Sinorhizobium meliloti 1021”
Feng Chi et al., Proteomics 10 (2010), 1861-1874
Data are based on the average linear root and shoot growth of three
symbiotic (dashed line) and three nonsymbiotic (solid line) plants.
Arrows indicate the times when root hair development started.
Ratio of root and shoot growth in symbiotic and
nonsymbiotic rice plants -- seeds were inoculated
with the fungus Fusarium culmorum vs. controls
R. J. Rodriguez et al., ‘Symbiotic regulation of plant growth,
development and reproduction” Communicative
and Integrative Biology, 2:3 (2009).
Growth of nonsymbiotic (on left) and symbiotic (on right) rice seedlings.
On the growth of endophyte (F. culmorum) and plant inoculation procedures,
see Rodriguez et al., Communicative and Integrative Biology, 2:3 (2009).
More productive phenotypes also can give
higher water-use efficiency as reflected in the
ratio of photosynthesis to transpiration
For each 1 millimol of water lost by transpiration:
3.6 millimols of CO2 are fixed in SRI plants,
1.6 millimols of CO2 are fixed in RMP plants
This is ever more important with climate change
“An assessment of physiological effects of the System of Rice
Intensification (SRI) compared with recommended rice cultivation
practices in India,” A.K. Thakur, N. Uphoff and E. Antony
Experimental Agriculture, 46(1), 77-98 (2010)
Economics, environmental vulnerabilities,
and climate change effects will all require a
different kind of agriculture in 21st century.
We need to RE-BIOLOGIZE AGRICULTURE
Fortunately, opportunities for a paradigm shift
are available -- but they will require significant
changes in our crop and soil sciences, with work
in disciplines of microbiology, physiology, soil
ecology, and epigenetics becoming more central
Closing thought: Darwin’s ‘tree of life’ was
good taxonomy, but not very good biology --
need to appreciate inhabitants of ‘inner space’
For more information on SRI/SCI:
SRI International Network and
Resources Center (SRI-Rice)
Website: http://sri.ciifad.cornell.edu
based at Cornell International Institute
for Food, Agriculture and Develoment
(CIIFAD), Cornell University, or contact
Norman Uphoff: ntu1@cornell.edu

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1306- Insights into Plant-Microbial Symbiosis and Implications for Sustainable Agriculture

  • 1. Insights into Plant-Microbial Symbiosis and Implications for Sustainable Agriculture – Giving Attention to ‘Inner Space’ Norman Uphoff, SRI-Rice, Cornell University National Institute for Agricultural and Forestry Research (IDIAP), Santo Domingo, January 26, 2013
  • 2. A challenge for our 21st century agriculture is to produce MORE with LESS Necessary to achieve sustainable development • This may sound impossible or improbable • However, it may be achieved by working more successfully within the realm of BIOLOGY, which operates differently from the realms of chemistry and engineering – can be ‘win-win’ Transformation of inputs into outputs is a generic process; however, BIOLOGY operates within open systems with options for mobilizing energy and nutrients that are otherwise unutilized or underutilized
  • 3. In the 21st century agriculture, we cannot just do ‘more of the same’ • Arable land area per capita is reducing as • Populations continue to grow, while • Land area is being lost to urban spread, and • Land degradation is increasing year by year • Water supply for agriculture is declining • Competing demands for domestic use and industry • Climate change is reducing amount and reliability • Pests and diseases are likely to increase In the US, crop losses to insects rose from 7% to 13%, while the use of insecticides was increased by 14x
  • 4. • Future energy prices will be higher in this centure than in the 20th century, affecting: • Production costs: fuel, fertilizer, agrochemicals • Transport cost: long-distance trade more costly • Climate patterns will become less favorable • Impact will be greatest in poorest countries • Accessibility of technology remains big issue • The Green Revolution by-passed most of the world’s poor ; must enable them to meet needs • Scale-neutral technologies are most desirable • Agric. productivity gains have slowed down
  • 5.
  • 6. GREEN REVOLUTION TECHNOLOGY was based on two main factors: A. Improvements in GENETIC POTENTIALS, i.e., in crop and animal genotypes (varieties) B. Increasing application of EXTERNAL INPUTS -- inorganic fertilizers, biocides, etc. These elements were successful in the past, but: • Economic costs of production are increasing, • Environmental costs are increasing, and now • Diminishing returns are evident, e.g., in China, the ratio of additional rice production from 1 kg of N has fallen from 20:1 to 5:1, and still declining
  • 7. Where do we go from here? More of the same, but better? Green Revolution was shaped more by chemistry, engineering and genetics than by biology (physiology and microbiology) and by ecology It ignored the contributions made by plant roots and by the soil biota
  • 8. Our challenge for sustainable agriculture is to produce MORE OUTPUT with REDUCED INPUTS learning how to get more productive PHENOTYPES from available GENOTYPES – can be done by making beneficial changes in crops’ growing environments The System of Rice Intensification (SRI) developed in Madagascar has shown how farmers can get more productive rice plants from existing varieties (local, HYVs, hybrids) at same time giving crops more resistance to effects of CLIMATE-CHANGE: • More DROUGHT resistance • Resistance to STORM DAMAGE (less lodging) • More resistance to PEST & DISEASE HAZARDS • Even some tolerance of temperature extremes Its methods are being adapted to many OTHER CROPS
  • 9. The Basic Ideas for SRI/SCI: • Establish healthy plants early (young) and carefully, making efforts to maintain their root growth potential. • Reduce plant density, giving each plant more room to grow, both above-ground and below-ground, to capture more sunlight and obtain more soil nutrients. • Keep the soil well-aerated and enriched with organic nutrients, as much as possible, so that it can support better growth of roots and more aerobic soil biota. – Apply water in ways that can best support the growth of plant roots and of beneficial soil microbes, avoiding continuous inundation and anaerobic soil conditions. – Control weeds in soil-aerating way (mechanical weeder). When used together, these practices enable farmers to: (a) increase the size and functioning of ROOT SYSTEMS, and (b) enhance the populations of beneficial SOIL BIOTA.
  • 10. Farmer with a rice plant grown from a single seed with SRI methods in Morang district of NEPAL
  • 11. Farmer with two plants of same variety (VN 2084) and same age (52 DAS) in CUBA
  • 12. Comparison trials at Al-Mishkhab Rice Research Station, Najaf, in IRAQ
  • 13. SRI 0 50 100 150 200 250 300 IH H FH MR WR YRStage Organdryweight(g/hill) IH H FH MR WR YR CK Yellow leaf and sheath Panicle Leaf Sheath Stem 47.9% 34.7% Non-Flooding Rice Farming Technology in Irrigated Paddy Field Dr. Tao Longxing, China National Rice Research Institute, 2004
  • 14. SRI methods have set a new world record Paddy production: Bihar panchayat breaks China’s record New Delhi, Mar 20: A gram panchayat in Nalanda district of Bihar has surpassed the Chinese record of paddy production, the Union Agriculture Minister Mr Sharad Pawar informed Parliament today. “As per the reports received from the state government, the yield of wet paddy has been recorded at 22.4 tonnes per hectare and that of dry paddy at 20.16 tonnes a hectare ...,” Mr Pawar said in a written reply to Lok Sabha. The record yield was achieved under demonstration on System of Rice Intensification (SRI) which was organised at farmer’s field during kharif 2011, he added. “It has surpassed the yield of 19 tonnes per hectare which was recorded earlier in China.”
  • 15. Before 1999: Madagascar 1999-2000: China, Indonesia 2001-02: Bangladesh, Cuba, Laos, Cambodia, Gambia, India, Nepal, Myanmar, Philippines, Sierra Leone, Sri Lanka, Thailand 2003: Benin, Guinea, Mozambique, Peru 2004-05: Senegal, Pakistan, Vietnam 2006: Burkina Faso, Bhutan, Iran, Iraq, Zambia 2007: Afghanistan, Brazil, Mali 2008: Rwanda, Costa Rica, Egypt, Ecuador, Ghana, Japan 2009: Malaysia, Timor Leste 2010: Kenya, DPRK, Panama, Haiti 2011: Colombia, Korea, Taiwan, Tanzania 2012: Burundi, Dominican Republic, Niger, Nigeria, Togo (total of 51) 2012: >50 countries of Asia, Africa, and Latin America where SRI’s phenotypic benefits have been seen
  • 16. Agroecological methods can give significant increases in yield, by multiples rather than increments, for resource-limited households with reduced inputs (seeds, water, fertilizer) * ‘Intensification’ is of farmer’s knowledge, skill and management -- rather than of purchased inputs – but also, with mechanization it is possible to save labor * Changes are made in the management of plants, soil, water and nutrients to affect the populations and activity of soil biota
  • 17. INDONESIA Caritas introduced SRI methods in Aceh in 2005 after tsunami devastation – local rice yields were raised from 2 t/ha to 8.5 t/ha “Using less rice seed, less water and organic compost, farmers in Aceh have quadrupled their crop production.” ‘Rice Aplenty in Aceh,’ Caritas News (2009) Similar quadrupling of yield by poor, food-insecure, resource- limited households has been documented also in Madagascar, Cambodia, and Madhya Pradesh (India)
  • 18. INDIA: Report in The HINDU Nov. 28, 2011 on SRI results in Madhya Pradesh SRI methods were introduced in Damoh district of Madhya Pradesh state by Gramin Vikas Samiti, with support from the People’s Science Institute (PSI) More than 1,200 farmers in 32 villages increased their average paddy yields from 1.7-2.0 t/ha to 7.5-8.0 t/ha with minimum of 4.4 t/ha and maximum of 11.5 t/ha -- using traditional varieties and with organic management SRI panicle with traditional variety (top); HYV panicle with usual mgmt (bottom)
  • 19. Hang Hein’s field was transplanted in one day by his 3 sons below; traditional transplanting methods are shown on right; with SRI crop management, Hang Hein’s yield went from 1.25 t/ha to 5 t/ha CAMBODIA: SRI introduced in Kampong Chhnang province in 2006-2007 by LDS Charities, with 146 farmers whose rainfed yields had previously averaged just 1.06 t/ha -- their yields with SRI practices averaged 4.02 t/ha
  • 20. These changes in crop management are effective in very different and quite contrasting agroecosystems: * AFGHANISTAN: Baghlan province 1600 masl, temperate climate; short growing season * MALI: Timbuktu province on edge of Sahara Desert; hot, dry tropical climate
  • 21. AFGHANISTAN: SRI field in Baghlan Province, supported by Aga Khan Foundation Natural Resource Management program
  • 22. AKF technician making a field visit in Baghlan province
  • 23. SRI field at 30 days
  • 24. SRI plant with 133 tillers @ 72 days after transplanting 11.56 t/ha
  • 25. * Some areas could not continue or be measured because of Taliban SRI yields were achieved with reductions in water Year SRI Users SRI Yield Conv. Yield 2008 6 10.1 5.4 2009 42 9.3 5.6 2nd yr [7] [13.3] [5.6] 1st yr [35] [8.7] [5.5] 2010 104 8.8 5.6 2011 114* 10.01 5.04
  • 26. MALI -- SRI nursery in Timbuktu region – 8-day seedlings ready for transplanting
  • 27. SRI transplanting on edge of Sahara Desert
  • 28. Malian farmer in the Timbuktu region showing the difference between regular and SRI rice plants with 32% less water Gao region: 7.84 t/ha Mopti region: 7.85 t/ha Year SRI Users SRI Yield Conv. Yield 2007-08 1 8.98 -- 2008-09 60 9.01 5.49 2009-10 130 7.71 4.48
  • 29. Environmental Benefits with SRI: 1. Reduced water requirements – higher crop water-use efficiency -- puts less pressure on ecosystems in competition with agriculture for water supplies 2. Higher land productivity – reducingpressures for the expansion of arable area to feed our populations 3. Less use of inorganic fertilizer – reactive N is “the third major threat to our planet after biodiversity loss and climate change” (John Lawton, former chief executive, UK National Environmental Research Council) 4. Less reliance on agrochemicals for crop protection - which enhances the quality of both soil and water 5. Buffering the effects of climate change – drought, storms (resist lodging), cold temperatures, etc. 6. Possible reduction in greenhouse gases (GHG) – CH4 is reduced apparently without producing offsetting N2O
  • 30. Other Benefits from Changes in Practices 1. Water saving – major concern in many places, also now have ‘rainfed’ version with similar results 2. Greater resistance to biotic and abiotic stresses – less damage from pests and diseases, drought, typhoons, flooding, cold spells [discuss tomorrow] 3. Shorter crop cycle – same varieties are harvested by 1-3 weeks sooner, save water, less crop risk 4. High milling output – by about 15%, due to fewer unfilled grains (less chaff) and fewer broken grains 5. Reductions in labor requirements – widely reported incentive for changing practices in India and China; also, mechanization is being introduced many places 6. Reductions in costs of production – greater farmer income and profitability, also health benefits Drought-resistance: Rice fields in Sri Lanka, same variety and same soil 3 weeks after irrigation had stopped because of drought – conventional rice field (left) and SRI (right)
  • 31. INDIA: Results from Bihar State, 2007-2012 SYSTEM OF RICE INTENSIFICATION -- state average yield: 2.3 t/ha 2007 2008 2009 2010 2012 Climatic conditions Normal rainfall 2x flooding Drought + rain in Sept. Complete drought Good rainfall No. of smallholders 128 5,146 8,367 19,911 NR Area under SRI (ha) 30 544 786 1,412 335,000 SRI yield (t/ha) 10.0 7.75 6.5 3.22* 8.08 Conv. yield (t/ha) 2.7 2.36 2.02 1.66* NR , SYSTEM OF WHEAT INTENSIFICATION -- state average yield: 2.4 t/ha 2007-08 2008-09 2009-10 2011-12 No. of smallholders 415 25,235 48,521 NR Area under SWI (ha) 16 1,200 2,536 183,085 SWI yield (t/ha) 3.6 4.5 NA 5.1 Conv. yield (t/ha) 1.6 1.6 NA NR * Results from measurements of yield on 74 farmers’ SRI and conventional fields
  • 32. Year 2004 2005 2006 2007 2008 2009 2010 Total SRI area (ha) 1,133 7,267 57,400 117,267 204,467 252,467 301,067 941,068 SRI yield (kg/ha) 9,105 9,435 8,805 9,075 9,300 9,495 9,555 9,252 Non-SRI yield (kg/ha) 7,740 7,650 7,005 7,395 7,575 7,710 7,740 7,545 SRI increment (t/ha)* 1,365 1,785 1,800# 1,680 1,725 1,785 1,815# 1,708 SRI % yield increase * 17.6% 23.3% 25.7% 22.7% 22.8% 23.2% 23.5% 22.7% Grain increase (tons) 1,547 12,971 103,320 197,008 352,705 450,653 546,436 1.66 mill Addl. net income from SRI use (million RMB)* 1.28 11.64 106.5 205.1 450.8 571.7 704.3 2,051 (>$300 mill) * Comparison with Sichuan provincial average for paddy yield and SRI returns # Drought years: SRI yields were relatively better than with conventional methods Source: Data are from the Sichuan Provincial Department of Agriculture. CHINA: SRI extension/impact in Sichuan Province, 2004-10
  • 33. Storm resistance: Dông Trù village, Ha Noi province, Vietnam, after fields were hit by a tropical storm Right: conventional field and plant; Left: SRI field and plant Same variety used in both fields: serious lodging seen on right -- no lodging on left
  • 34. Irrigation method Seedling age Spacing (cm2) Plant lodging (in percent) Partial Complete Total Inter- mittent irrigation (AWDI) 14 30x30 6.67 0 6.67 30x18 40.00 6.67 46.67 21 30x30 26.67 20 46.67 30x18 13.33 13.33 26.67 Ordinary irrigation (continuous flooding) 14 30x30 16.67 33.33 50.00 30x18 26.67 53.33 80.00 21 30x30 20 76.67 96.67 30x18 13.33 80 93.33 Lodging of rice as affected by irrigation practices when combined with different ages of seedlings and different spacings in trials done in Chiba, Japan (Chapagain and Yamaji, Paddy and Water Environment, 2009)
  • 35. Disease and pest resistance: Evaluation by Vietnam National IPM Program, 2005-06 – averages of data from on-farm trials in 8 provinces Spring season Summer season SRI plots Farmer plots Differ- ence SRI plots Farmer plots Differ- ence Sheath blight 6.7% 18.1% 63.0% 5.2% 19.8% 73.7% Leaf blight -- -- -- 8.6% 36.3% 76.5% Small leaf folder * 63.4 107.7 41.1% 61.8 122.3 49.5% Brown plant hopper * 542 1,440 62.4% 545 3,214 83.0% AVERAGE 55.5% 70.7% * Insects/m2
  • 36. Resistance to both biotic and abiotic stresses: fields in East Java, Indonesia hit by both brown planthopper (BPH) and by storm damage (typhoon): rice field on left was managed with standard practices; organic SRI is seen on right Modern improved variety (Ciherang) – no yield Traditional aromatic variety (Sintanur) - 8 t/ha
  • 37. Resistance to cold temperature: Yield and meteorological data from ANGRAU, A.P., India Period Mean max. temp. 0C Mean min. temp. 0C No. of sunshine hrs 1 – 15 Nov 27.7 19.2 4.9 16–30 Nov 29.6 17.9 7.5 1 – 15 Dec 29.1 14.6 8.6 16–31 Dec 28.1 12.2# 8.6 # Sudden drop in minimum temp. for 5 days (16–21 Dec = 9.2-9.9o C ) Season Normal (t/ha) SRI (t/ha) Kharif 2006 0.21* 4.16 Rabi 2005-06 2.25 3.47 * Low yield was due to cold injury (see below)
  • 38. Comparison of methane gas emission CT SRI kgCH4/ha 0 200 400 600 800 1000 840.1 237.6 72 % Treatment Emission (kg/ha) CO2 ton/ha equivalentCH4 N2O CT 840.1 0 17.6 SRI 237.6 0.074 5.0
  • 39. SRI practices are being used beyond RICE: Farmer-led innovations with civil society help in: • Wheat (SWI) -- India, Nepal, Ethiopia, Mali • Sugarcane (SSI) -- India, Cuba • Finger millet (SFMI) -- India, Ethiopia • Mustard/rapeseed/canola (SMI) -- India • Teff (STI) -- Ethiopia • Sorghum (SSI2) – Ethiopia • Turmeric (STI2) -- India System of Crop Intensification (SCI): maize, black gram, green gram, red gram, tomatoes, chillies, eggplant, sesame, etc. -- India, Ethiopia
  • 40.
  • 41.
  • 42.
  • 43. Wheat: SWI (left) vs. conventional plants in Bihar, India
  • 45. Tef: Application of SRI concepts & practices to production of tef (STI) in Ethiopia Left: transplanted tef Right: broadcasted tef 3-5 t/ha vs. 1 t/ha
  • 46. STI tef crop in Tigray province of Ethiopia
  • 47. ICRISAT-WWF Sugarcane Initiative: • 20-100% more cane yield, with • 30% reduction in water, and • 25% reduction in chemical inputs “The inspiration for putting this package together is from the successful approach of SRI – System of Rice Intensification.”
  • 48. Sugarcane: SSI cane plants seen in India – SSI is now getting started in Cuba, known as SiCAS
  • 49. CUBA: SicAS sugarcane @ 10.5 months Eventual yield was estimated @ 150 t/ha
  • 50. Crops Yield increases Finger millet 3-4x Legumes 50-200% Maize 75% Mustard 3-4x Sugarcane 20-100% Tef 3-5x Turmeric 25% Vegetables 100-270% Wheat 10-140% SCI crops are mostly rainfed, but 30% water-saving with wheat and sugarcane, 66% with turmeric Summary of results reported from farmers' fields for System of Crop Intensification (SCI) applying SRI concepts and methods to other crops
  • 51. These results do NOT argue against making further genetic improvements or against the use of external inputs They suggest, however, that progress can be made right now at low cost -- with saving of water & buffering against climate change -- by changing crop management practices, especially by attending to the purposeful nurturing of roots and soil biota WHAT IS GOING ON?
  • 52. SRI/SCI shows us the importance of abundance, diversity and activity of beneficial SOIL ORGANISMS promoted by soil organic matter and by exudates from large, functioning ROOT SYSTEMS that support plant growth and health We are just starting to understand better the contributions of symbiotic endophytes to mobilizing the services of plant microbiomes that aid crops
  • 53. Soil-aerating hand weeder in Sri Lanka costing <$20
  • 54. Effects of Active Soil Aeration 412 farmers in Morang district of Nepal when using SRI in monsoon season, 2005 SRI yield = 6.3 t/ha vs. control yield = 3.1 t/ha Data show how WEEDINGS can raise yield No. of No. of Average Range weedings farmers yield of yields 1 32 5.16 (3.6 - 7.6) 2 366 5.87 (3.5 - 11.0) 3 14 7.87 (5.85 - 10.4)
  • 55. Mechanical Weedings Farmers (N) Area (ha) Harvest (kg) Yield (t/ha) 0 2 0.11 657 5.973 1 8 0.62 3,741 7.723 2 27 3.54 26,102 7.373 3 24 5.21 47,516 9.120 4 15 5.92 69,693 11.772 Impact of weedings on yield with SRI methods in Ambatovaky, Madagascar, 1997-98
  • 56. ENDOPHYTIC AZOSPIRILLUM, TILLERING, AND RICE YIELDS WITH CULTIVATION PRACTICES AND NUTRIENT AMENDMENTS Replicated trials at Anjomakely, Madagascar, 2001 (Andriankaja, 2002) CLAY SOIL Azospirillum in roots (103 CFU/mg) Tillers/ plant Yield (t/ha) Conventional methods, with no soil amendments 65 17 1.8 SRI cultivation, with no soil amendments 1,100 45 6.1 SRI cultivation, with NPK fertilizer 450 68 9.0 SRI cultivation, with compost 1,400 78 10.5 LOAM SOIL SRI cultivation with no soil amendments 75 32 2.1 SRI cultivation, with compost 2,000 47 6.6
  • 57. Microbial populations in rice rhizosphere Tamil Nadu Agricultural University research Microorganisms Conventional methods SRI methods Total bacteria 88 x 106 105 x 106 Azospirillum 8 x 105 31 x 105 Azotobacter 39 x 103 66 x 103 Phosphobacteria 33 x 103 59 x 103 T. M. Thiyagarajan, WRRC presentation, Tsukuba, Japan, 2004
  • 58. Total bacteria Total diazotrophs Microbial populations in rhizosphere soil in rice crop under different management at active tillering, panicle initiation, and flowering (conv. = red; SRI = yellow). Units are √ transformed values of population/gram of dry soil (data from IPB) Phosphobacteria Azotobacter 0 10 20 30 40
  • 59. Dehydrogenase activity (μg TPF) Urease activity (μg NH4-N)) Microbial activities in rhizosphere soil in rice crop under different management (conv. = red; SRI = yellow) at active tillering, panicle initiation, and flowering stages Units are √ transformed values of population/gram of dry soil per 24 h Acid phosphate activity (μg p-Nitrophenol) Nitrogenase activity (nano mol C2H4)
  • 60. Effects of symbiotic microorganisms in rice plants go beyond the root zone (the rhizosphere) They also extend upward into the shoot & leaves (phyllosphere) and even seeds Contributions made by symbiotic endophytes are just starting to be well documented and widely known
  • 61. “Ascending Migration of Endophytic Rhizobia, from Roots and Leaves, inside Rice Plants and Assessment of Benefits to Rice Growth Physiology” Feng Chi et al., Applied and Envir. Microbiology 71 (2005), 7271-7278 Rhizo- bium strain Total plant root vol/pot (cm3) ± SE Shoot dry wt/pot (g) ± SE Net photosyn- thesis rate (µmol of CO2 m-2 s-1) ± SE Water utilization efficiency ± SE Grain yield/pot (g) ± SE Ac-ORS 571 210 ± 36A 63 ± 2A 16.42 ± 1.39A 3.63 ± 0.17BC 86 ± 5A Sm-1021 180 ± 26A 67 ± 5A 14.99 ± 1.64B 4.02 ± 0.19AB 86 ± 4A Sm-1002 168 ± 8AAB 52 ± 4BC 13.70 ± 0.73B 4.15 ± 0.32A 61 ± 4B R1-2370 175 ± 23A 61 ± 8AB 13.85 ± 0.38B 3.36 ± 0.41C 64 ± 9B Mh-93 193 ± 16A 67 ± 4A 13.86 ± 0.76B 3.18 ± 0.25CD 77 ± 5A Control 130 ± 10B 47 ± 6C 10.23 ± 1.03C 2.77 ± 0.69D 51 ± 4C
  • 62. “Proteomic analysis of rice seedlings infected by Sinorhizobium meliloti 1021” Feng Chi et al., Proteomics 10 (2010), 1861-1874
  • 63. Data are based on the average linear root and shoot growth of three symbiotic (dashed line) and three nonsymbiotic (solid line) plants. Arrows indicate the times when root hair development started. Ratio of root and shoot growth in symbiotic and nonsymbiotic rice plants -- seeds were inoculated with the fungus Fusarium culmorum vs. controls R. J. Rodriguez et al., ‘Symbiotic regulation of plant growth, development and reproduction” Communicative and Integrative Biology, 2:3 (2009).
  • 64. Growth of nonsymbiotic (on left) and symbiotic (on right) rice seedlings. On the growth of endophyte (F. culmorum) and plant inoculation procedures, see Rodriguez et al., Communicative and Integrative Biology, 2:3 (2009).
  • 65. More productive phenotypes also can give higher water-use efficiency as reflected in the ratio of photosynthesis to transpiration For each 1 millimol of water lost by transpiration: 3.6 millimols of CO2 are fixed in SRI plants, 1.6 millimols of CO2 are fixed in RMP plants This is ever more important with climate change “An assessment of physiological effects of the System of Rice Intensification (SRI) compared with recommended rice cultivation practices in India,” A.K. Thakur, N. Uphoff and E. Antony Experimental Agriculture, 46(1), 77-98 (2010)
  • 66. Economics, environmental vulnerabilities, and climate change effects will all require a different kind of agriculture in 21st century. We need to RE-BIOLOGIZE AGRICULTURE Fortunately, opportunities for a paradigm shift are available -- but they will require significant changes in our crop and soil sciences, with work in disciplines of microbiology, physiology, soil ecology, and epigenetics becoming more central Closing thought: Darwin’s ‘tree of life’ was good taxonomy, but not very good biology -- need to appreciate inhabitants of ‘inner space’
  • 67. For more information on SRI/SCI: SRI International Network and Resources Center (SRI-Rice) Website: http://sri.ciifad.cornell.edu based at Cornell International Institute for Food, Agriculture and Develoment (CIIFAD), Cornell University, or contact Norman Uphoff: ntu1@cornell.edu